Nama : Novian Wildan R.

NIM : K4318044

Kelas : B

UTS EVOLUSI

1. Carilah beberapa definisi evolusi oleh beberapa ahli, sertakan nama dan
tahunya. Lakukan identifikasi kata kunci di setiap definisi tersebut, lalu
sintesislah dari berbagai kata kunci definisi menjadi sebuah pengertian
tentang evolusi.

Jawab:

a. Teori lamarck (1744-1829)

Menurut Jean Baptisk Lamarck evolusi akan muncul ketika adanya
suatu adaptasi, sedangkan penyebab munculnya adaptasi adalah
suatuproses penyesuaian makhluk hidup dengan lingkungan yang
kemudian akan diwariskan kepada generasi berikutnya atau
keturunannya. Konsep yang terkenal adalah use dan disuse pada organ-
organ makhluk hidup yang memiliki arti dipergunakan atau tidak
dipergunakan dan itu akan berlaku kekal sehingga dapat menurunkan
kepada keturunannya (Mawardi & Hidayati, 2009).
b. Teori darwin (1809-1882)
Charles darwin tidak sependapat dengan gagasan Lamarck, dia
mengemukakan bahwa evolusi terjadi karena adanya seleksi alam.
Bahwasanya spesies yang hidup pada saat ini, adalah bermula dari
spesies masa lampau. Gagasan itu dikemukakan dalam bukunya The
Original of species by Means of Selection or The reservation of Favoured
Races in the Struggle for Life Mawardi & Hidayati, 2009).
c. Teori Alfred Wallace (1823-1913)
Selain Darwin ternyata ada seorang ilmuan yang mengemukakan
gagasannya tentang evolusi yang serupa dan itu adalah Wallace.
 Pengamatan Wallace berlangsung di berbagai benua dan termasuk pula di
Sulawesi yang terkenal dengan garis Wallace sebagai garis pemisah.
d. Teori Hugo De Vries (1848-1935)
Seorang botanikus asal Belanda dia adalah De Vries, yang
mengungkapkan bahwa evolusi itu terjadi karena adannya mutasi. Mutasi
adalah perubahan yang sempurna terhadap sifat dalam keturunannya
(Mawardi & Hidayati, 2009).
e. Teori August wiesmann (1834-1914)
Weismann berpendapat sama dengan gagasan yang dimiliki
Darwin, dia menambahi gagasan darwin dengan pernyataan seperti ini:
bahwasanya evolusi yaitu masalah genetika yang memiliki artian tentang
keturunan yang menyangkut masalah bagaimanakah mewariskan gen-gen
melalui sel kelamin. Sel-sel yang ada ditubuh tidak dipengaruhi oleh
suatu kondisi lingkungan, jadi evolusi menurut weismannmerupakan hal
yang mempengaruhi genetika makhluk hidup melalui seleksi alam.
(Mawardi & Hidayati, 2009).

Dari beberapa pendapat para ahli di atas dapat disimpulkan bahawa evolusi
merupakan suatu peristiwa yang terjadi karena penyesuaian kondisi akibat dari
adanya seleksi alam sehingga dapat mengakibatkan mutasi gen atau terjadi
perubahan gen gen pada makhluk hidup.

Referensi :
Mawardi, & Hidayati, N. (2009). Ilmu Alamiah Dasar Ilmu Sosial Dasar Ilmu
Budaya Dasar IAD-ISD-IBD. Bandung: CV Pustaka Setia.

2. Lakukan kajian literatur tentang pembagian evolusi (setiap pembagian

memiliki dasar, misalnya berdasarkan arahnya evolusi dibagi menjadi
progresif dan regresif, dan seterusnya) buatlah uraian tentang pembagian
evolusi ini sekomplit mungkin dari berbagai literatur, sertakan nama
author dan tahun terbit literatur tersebet.

Jawab:
 a) Berdasarkan Arahnya

Berdasarkan arahnya evolusi dibagi menjadi dua yaitu evolusi progresif dan
evolusi regresif (retrogresif). Evolusi progresif menitikberatkan pada hasil akhir,
yaitu makhluk hidup dapat bertahan hidup pada lingkungannya (survive), proses
ini dapat dijumpai melalui peristiwa evolusi yang terjadi pada burung Finch.
Sedangkan evolusi regresif memiliki kecenderungan pada kepunahan dari
makhluk hidup yang mengalami evolusi karena tidak mampu menyesuaikan diri
dengan kondisi lingkungannya. Ke dua macam evolusi tersebut, pada dasarnya
dibagi berdasarkan pada pengaruh akhir dari proses evolusi yang terjadi, yaitu
bertahan karena mampu beradaptasi atau punah karena tidak mampu beradaptasi
dengan perubahan lingkungan yang terjadi. (Arbi, 2012)

b) Berdasarkan Skala Perubahannya

Berdasarkan skala perubahannya, evolusi dibagi menjadi 2 yaitu makroevolusi

dan mikro evolusi. Makroevolusi adalah evolusi yang terjadi pada tingkat spesies,
seperti kepunahan dan spesiasi. Wujud dari makroevolusi adalah ciri-ciri fenotip
yng terekspresikan misalnya morfologi tubuh, anatomi dan struktur organ,
perilaku, serta ekspresi fisiologis. Sedangkan mikroevolusi adalah peristiwa
terjadinya perubahan skala kecil pada frekuensi alel suatu populasi selama
beberapa generasi. Ia juga disebut sebagai perubahan dibawah tingkat spesies.
Secara umum makroevolusi dianggap sebagai akibat jangka panjang dari
mikroevolusi. Sehingga perbedaan antara makroevolusi dan mikroevolusi tidaklah
begitu banyak terkecuali pada waktu yang terlibat dalam proses tersebut. Namun
pada makroevolusi, sifat-sifat keseluruhan karakteristik spesies merupakan hal
yang penting. Misalnya adanya variasi sifat sifat di antara individu
memungkinkan suatu spesies secara cepat beradaptasi terhadap habitat yang baru,
sehingga mengurangi kemungkinan terjadinya kepunahan. (Leksono, 2012)

c) Berdasarkan Hasil Akhir

Berdasarkan hasil akhir evolusi dibagi menjadi dua yaitu evolusi konvergen
dan evolusi divergen. Evolusi konvergen merupakan evolusi independen yang
menyebabkan kemiripan karakter pada spesiesdengan kekerabatan yang berbeda.
Evolusi konvergen menciptakan struktur analogis dengan fungsi yang sama,
namun tidak terdapat pada leluhur kelompok taksa tersebut. Fenomena tersebut
seringkali merupakan akibat dari hasil pengaruh lingkungan hidup yang serupa
dan mengisi niche ekologi yang sama. Struktur atau bentuk tubuh yang mirip
tersebut dalam hal ini dikenal sebagai struktur analog. Fenomena evolusi
konvergen seringkali terlihat pada Passeriformes yang merupakan ordo dengan
jumlah anggota terbesar dari kelas Aves.

Kebalikan dari evolusi konvergen, evolusi divergen adalah munculnya

beberapa spesies yang memiliki bentuk morfologi sangat bervariasi dan berasal
dari garis keturunan yang sama, spesies-spesies tersebut memiliki ciri-ciri yang
sama karena mereka adalah keturunan dari satu nenek moyang tunggal. Ciri-ciri
yang masih diwarisi dari leluhur mereka dikenal sebagai struktur homolog. [misal:
struktur dasar kerangka yang mirip di antara hewan vertebrata pada tahap embrio].
Struktur homolog serupa dalam struktur dan fungsi karena mereka berasal dari
nenek moyang yang sama.

Sumber :

Arbi U. Y. (2012), Sejarah Dan Bukti Evolusi Pada Gastropoda. Jurnal Oseana,
Vol. XXXVII, No. 2

Kurniawan A. dan Arifianto A. (2017). Ornitologi: Sejarah, Biologi

dan Konservasi. Malang: UB Press

Leksono A.S. (2012). Sejarah Kehidupan: Perspektif Evolusi dan Kreasi. Malang:
UB Press

3. Lakukan hal yang sama untuk sejarah perkembangan teori evolusi sejak
sebelum darwin sampai sekarang. Lakukan analisis persamaan atau
dukungan dan perbedaanya dengan teori evolusi Darwin.

Jawab:

 Masa Pra Darwin

 Pada masa pra Darwin, teori evolusi organik memperkirakan bahwa sejak
kehidupan muncul di bumi, telah terjadi suatu proses berkesinambungan.
Organisme yang hidup berasal dari bentuk-bentuk sebelumnya. Variasi-variasi
yang besar adalah sabagai hasil respons makhluk hidup terhadap perubahan
lingkungan. Respons ini berupa perubahan struktur dan fungsi tubuh makhluk
individu hidup yang kemudian dilangsungkan kepada generasi selanjutnya melalui
suatu proses pewarisan sifat yang telah mengalami perubahan itu.

 Masa Darwin
o Masa Seleksi Alam (Darwin, Wallace)

Organisme di bumi yang beraneka ragam itu merupakan hasil dari seleksi alam.
Kondisi alam yang selalu berubah (dinamik), baik yang berupa faktor nirhayat
(abiotik) maupun hayat (biotik), adalah sebagai penyeleksi. Individu yang mampu
menyesuaikan diri (karena kuat, tahan penyakit, dsb) terhadap perubahan alam
akan dapat bertahan hidup, sedangkan yang tidak mampu akan terseleksi
(tereliminasi, mati). Struktur dan fungsi tubuh makhluk yang telah lolos dari
seleksi merupakan sifat yang akan diwariskan kepada generasi penerusnya.

1. Charles Darwin

Menurut Darwin evolusi terjadi karena adanya seleksi alam (faktor alam yg
mampu menyeleksi makhluk hidup. Adaptasi merupakan penyebab terjadinya
seleksi alam (mekanisme seleksi alam).

2. Sir Alfred Russel Wallace

Ia juga menyatakan persetujuannya pada konsep Survival of the fittest (siapa yang
kuat dia yang menang) seperti yang dikemukakan oleh Darwin.

o Masa Teori Genetika (Mendel, De Vries, Tschernov, Bateson, Weismann).

1. Gregor Johan Mendel : Hukum Pewarisan Sifat

2. De Vries dan Tschernov : Perubahan sifat yang dilatarbelakangi oleh mutasi

gen-gen, dan kemudian diwariskan kepada keturunannya.
3. Bateson : Bahwa kesesuaian antara warna tubuh makhluk
hidup dengan lingkungannya, atau disebut mimikri, merupakan adaptasi dalam
bentuk warna penyamaran, sehingga tidak tampak mencolok.

4. Weismann (1834-1912) : Bahwa evolusi terjadi karena adanya seleksi alam

terhadap faktor genetis.

 Masa Pasca Darwin

Pada masa ini masyarakat ilmiah lebih komunikatif, dibandingkan pd masa

sebelumnya, sehingga para ahli bisa melihat keterkaitan antara ilmu satu dengan
lainnya. Penemuan oleh Hugo de Vries dan lainnya pada awal 1900-an
memberikan dorongan terhadap pemahaman bagaimana variasi terjadi pada sifat
tumbuhan dan hewan. Seleksi alam menggunakan variasi tersebut untuk
membentuk keanekaragaman sifat-sifat adaptasi yang terpantau pada organisme
hidup. Walaupun Hugo de Vries dan genetikawan pada awalnya sangat kritis
terhadap teori evolusi, penemuan kembali genetika dan riset selanjutnya pada
akhirnya memberikan dasar yang kuat terhadap evolusi, bahkan lebih meyakinkan
daripada ketika teori ini pertama kali diajukan.

Kontradiksi antara teori evolusi Darwin melalui seleksi alam dengan karya
Mendel disatukan pada tahun 1920-an dan 1930-an oleh biologiawan evolusi
seperti J.B.S. Haldane, Sewall Wright, dan terutama Ronald Fisher, yang
menyusun dasardasar genetika populasi. Hasilnya adalah kombinasi evolusi
melalui seleksi alam dengan pewarisan Mendel menjadi sintesis evolusi modern.
Bukan hanya Genetika dan Evolusi saja yang saling menunjang, tetapi semua
cabang ilmu biologi dapat menjelaskan fenomena evolusi. Pernyataan ini
didukung oleh sebagian besar ahli biologi pada waktu itu. Theodozius
Dobzhansky, ahli genetika, berjasa merangkum begitu banyak fenomena evolusi
dari berbagai macam disiplin biologi.

Sumber:

Campbell, N. A., J. B. Reece dan L.G. Mitchell. (1999). Biology. Fifth Edition.
New York : Addison Wesley Longman, Inc.
Prawoto, Sudjoko, Siti Mariyam. (1987). Evolusi. Jakarta : Universitas Terbuka,
Departemen pendidikan dan Kebudayaan.

4. Kajilah beberapa artikel yg menunjukkan adanya dinamika gen dalam

populasi. Tunjukkan temuan utama kajian tsb. Sertakan artikel
aslinya.

Jawab:

Pada artikel jurnal yang berjudul Variasi Genetik, Heritabilitas, dan Korelasi
Genotipik Sifat-Sifat Penting Tanaman Wijen (Sesamum indicum L.)
mengememukakan bahwa variasi genetik akan membantu dalam mengefisien- kan
kegiatan seleksi. Apabila variasi genetik dalam suatu populasi besar, maka akan
menunjukkan individu dalam populasi beragam sehingga peluang untuk
memperoleh genotip yang diharapkan akan besar. Penggunaan metode seleksi
merupakan proses yang efektif untuk memperoleh sifat–sifat yang dianggap
sangat penting dan tingkat keberhasilannya tinggi. Untuk mencapai tujuan seleksi,
harus diketahui antar karakter agronomi, komponen hasil dan hasil, sehingga
seleksi terhadap satu karakter atau lebih dapat dilakukan. Apabila variasi genetik
dalam suatu populasi besar, ini menunjukkan individu dalam populasi beragam
sehingga peluang untuk memperoleh genotip yang diharapkan akan besar

Pada jurnal ini dilakukan penelitian yang merupakan pengujian terhadap

genotip-genotip hasil persilangan tanaman wijen, dengan tujuan mendapatkan
informasi mengenai variasi genetik, heritabilitas, dan korelasi genotipik beberapa
sifat penting hasil persilangan tanaman wijen. Penelitian dilakukan di Kebun
Percobaan Pasirian, Lumajang, Jawa Timur pada bulan April 2002 – Agustus
2003. Rancangan yang digunakan adalah rancangan acak kelompok dengan tiga
ulangan. Hasil penelitian menunjukkan bahwa (1) sebagian besar sifat yang
diamati mempunyai variasi genetik yang cukup besar, (2) nilai heritabilitas (dalam
arti luas) tinggi terdapat pada sifat tinggi tanaman, umur berbunga, umur panen,
jumlah cabang per tanaman, jumlah polong per tanaman, panjang polong, berat
1000 biji, dan hasil biji per hektar, sehingga dapat digunakan sebagai kriteria
seleksi pada generasi awal, dan (3) korelasi genotipik terhadap hasil biji per
hektar terjadi pada sifat tinggi tanaman dan berat 1000 biji pada persilangan Sbr 1
X Si 13, sedangkan pada persilangan Sbr 1 X Si 22, dan Sbr 1 X Si 26 terjadi
korelasi genotipik antara hasil biji per hektar dengan tinggi tanaman dan jumlah
cabang per tanaman.
Jurnal Littri 13(3), September 2007. Hlm. 88 –J9U2RNAL LITTRI VOL. 13 NO. 3, SEPTEMBER 2007 : 88 - 92
ISSN 0853-8212
VARIASI GENETIK, HERITABILITAS, DAN KORELASI GENOTIPIK SIFAT-SIFAT
PENTING TANAMAN WIJEN (Sesamum indicum L.)
SUDARMADJI, RUSIM MARDJONO dan HADI SUDARMO
Balai Penelitian Tanaman Tembakau dan Serat
Jl. Raya Karangploso, Kotak Pos 199, Malang – Jawa Timur
ABSTRAK
Penelitian ini merupakan pengujian terhadap genotip-genotip hasil
persilangan tanaman wijen, dengan tujuan mendapatkan informasi
mengenai variasi genetik, heritabilitas, dan korelasi genotipik beberapa sifat
penting hasil persilangan tanaman wijen. Penelitian dilakukan di Kebun
Percobaan Pasirian, Lumajang, Jawa Timur pada bulan April 2002 –
Agustus 2003. Rancangan yang digunakan adalah rancangan acak kelom-
pok dengan tiga ulangan. Hasil penelitian menunjukkan bahwa (1) sebagian
besar sifat yang diamati mempunyai variasi genetik yang cukup besar, (2)
nilai heritabilitas (dalam arti luas) tinggi terdapat pada sifat tinggi tanaman,
umur berbunga, umur panen, jumlah cabang per tanaman, jumlah polong
per tanaman, panjang polong, berat 1000 biji, dan hasil biji per hektar,
sehingga dapat digunakan sebagai kriteria seleksi pada generasi awal, dan
(3) korelasi genotipik terhadap hasil biji per hektar terjadi pada sifat tinggi
tanaman dan berat 1000 biji pada persilangan Sbr 1 X Si 13, sedangkan
pada persilangan Sbr 1 X Si 22, dan Sbr 1 X Si 26 terjadi korelasi genotipik
antara hasil biji per hektar dengan tinggi tanaman dan jumlah cabang per
tanaman.
Kata kunci : Wijen, Sesamum indicum L., persilangan, genotip, variasi
genetik, heritabilitas, korelasi genotipik, pertumbuhan, hasil,
Jawa Timur
ABSTRACT
Genetic variations, heritability and genotypic correlations
of important characteristics of sesame (Sesamum indicum
L.)
The experiment was conducted to evaluate genetic variations,
heritability, and genotypic correlations of important characteristics of
sesame. The experiment was located at Pasirian Research Station,
Lumajang, East Java from April 2002 – August 2003. Randomized block
design with three replications was used in the experiment. The result of the
experiment showed that: (1) generally, the genetic variations for all traits
were high enough, (2) the heritability values (in broad sense) on plant
height, flowering time, harvest time, number of branches per plant, number
of pods per plant, length of pods, 1000-seed weight, and grain yield per
hectare were high, indicating that the inheritance of these traits were simple
inheritance and selection can be performed in early generation, and (3) in
Sbr 1 X Si 13 crosses, plant height and 1000-seeed weight had genotypic
correlation with grain yield per hectare, then plant height and number of
branches per plant had genotypic correlation with grain yield per hectare in
Sbr 1 X Si 22, and Sbr 1 X Si 26 crosses.
Key words : Sesame, Sesamum indicum L., crossing, genotype, genetic
variations, heritability, genotypic correlation, growth, yield,
East Java
PENDAHULUAN
Wijen merupakan tanaman penghasil biji yang
digunakan untuk pendukung utama aneka industri termasuk
88
industri makanan dan minyak makan yang berkadar lemak
jenuh rendah, sehingga cocok dikonsumsi bagi penderita
kolesterol tinggi (DESAI dan GOYAL, 1981). Minyak wijen
pada umumnya dapat digunakan sebagai minyak salad dan
minyak goreng. Di samping itu minyak wijen mengandung
anti oksidan, sesamin dan sesamolin, sehingga dapat
disimpan lebih dari satu tahun ( SUDDIYAM dan MANEEKHAO,
1997).
Di Indonesia produksi wijen mulai tahun 1987 mulai
menurun, sehingga pada tahun 1988 mengimpor sebesar
940.450 ton biji dan 133.729 ton minyak ( BPS, 2001).
Selanjutnya pada tahun 2001 sekitar 10.265 ton, sedangkan
produksi dalam negeri hanya 10.000 ton. Produktivitas
wijen di tingkat petani masih sangat rendah, rata-rata 350 kg
per hektar (SUPRIJONO et al., 1994). Hasil tersebut masih
sangat rendah bila dibandingkan dengan negara penghasil
wijen lainya. DESAI dan GOYAL (1981) menyatakan bahwa di
India mampu menghasilkan antara 1.200 – 1.400 kg per
hektar, sehingga produtivitas wijen di Indonesia perlu
ditingkatkan.
Salah satu usaha perbaikan wijen adalah dengan
melakukan seleksi pada suatu populasi dengan keragaman
genetik cukup tinggi. Apabila suatu karakter memiliki
keragaman genetik cukup tinggi, maka setiap individu
dalam populasi hasilnya akan tinggi pula, sehingga seleksi
akan lebih mudah untuk mendapatkan sifat-sifat yang
diinginkan. Oleh sebab itu, informasi keragaman genetik
sangat diperlukan untuk memperoleh varietas baru
yangdiharapkan (HELYANTO et al., 2000).
Metode seleksi merupakan proses yang efektif untuk
memperoleh sifat–sifat yang dianggap sangat penting dan
tingkat keberhasilannya tinggi (KASNO, 1992). Untuk
mencapai tujuan seleksi, harus diketahui antar karakter
agronomi, komponen hasil dan hasil, sehingga seleksi
terhadap satu karakter atau lebih dapat dilakukan ( ZEN,
1995).
Variasi genetik akan membantu dalam mengefisien-
kan kegiatan seleksi. Apabila variasi genetik dalam suatu
populasi besar, ini menunjukkan individu dalam populasi
beragam sehingga peluang untuk memperoleh genotip yang
diharapkan akan besar (BAHAR dan ZEIN, 1993). Sedangkan
pendugaan nilai heritabilitas tinggi menunjukkan bahwa
faktor pengaruh genetik lebih besar terhadap penampilan
fenotip bila dibandingkan dengan lingkungan. Untuk itu
informasi sifat tersebut lebih diperankan oleh faktor genetik
atau faktor lingkungan, sehingga dapat diketahui sejauh
mana sifat tersebut dapat diturunkan pada generasi
berikutnya.
 Korelasi dua atau lebih antar sifat positif yang di mana :
dimiliki akan memudahkan seleksi karena akan diikuti oleh 2f = ragam fenotip
peningkatan sifat yang satu diikuti dengan yang lainnya,
2g = ragam genetik
sehingga dapat ditentukan satu sifat atau indek seleksi
X = rata-rata
(ECKEBIL et al., 1977). Sebaliknya bila korelasi negatif,
umum
maka sulit untuk memperoleh sifat yang diharapkan. Bila
Berdasarkan kriteria MILIGAN et al. (1996), koefisien
tidak ada korelasi di antara sifat yang diharapkan, maka
keragaman genetik dibagi dalam tiga kategori yaitu :
seleksi menjadi tidak efektif (POESPODARSONO,1988).
- Besar (KVG  14,5%)
Penelitian ini bertujuan untuk memperoleh informasi - Sedang (5%  KVG < 14,5%)
mengenai variasi genetik, heritabilitas, dan korelasi geno-
- Kecil (KVG < 5%)
tipik sifat-sifat penting tanaman wijen. Hasil dari penelitian
ini sangat penting dalam program pemuliaan tanaman wijen.
Pendugaan nilai heritabilitas dalam arti luas untuk sifat-sifat
yang diamati, diduga dengan menggunakan rumus menurut
ALLARD, (1960) :

BAHAN DAN METODE 2F2 – (2P1 + 2P2 + 2F1)/3

h2 =
2F2
Penelitian dilakukan di Kebun Percobaan Tanaman di mana :
Tembakau dan Serat Pasirian, Kabupaten Lumajang, Jawa h2 = heritabilitas dalam arti luas
Timur dengan ketinggian 110 m di atas permukaan laut, 2F1 = ragam populasi F1
jenis tanah Regosol dengan pH 5,5 – 6,5. Penelitian 2F2 = ragam populasi F2
dilaksanakan bulan April 2002 – Agustus 2003. Rancangan 2P1 = ragam populasi P1
lingkungan yang digunakan dalam penelitian adalah 2P2 = ragam populasi P2
rancangan acak kelompok (RAK) dengan 10 genotip berasal
dari 4 genotip tetua yaitu P1 varietas Sbr 1 sebagai tetua Selanjutnya heritabilitas diklasifikasikan menurut MC
betina, P2 (galur Si 13), P3 (galur Si 22), dan P4 (galur Si WHIRTER, (1979), sebagai berikut:
26) sebagai tetua jantan, 3 genotip berasal dari F1 hasil - Tinggi (H  0,50)
persilangan Sbr 1 x Si 13, Sbr 1 x Si 22 dan Sbr 1 x Si 26, 3 - Sedang (0,20  H  0,50)
genotip berasal dari F2 hasil persilangan Sbr 1 x Si 13, Sbr - Kecil (H  0,20)
1 x Si 22 dan Sbr 1 x Si 26 diulang 3 kali sehingga
diperoleh 30 petak percobaan di mana setiap petak Untuk mengetahui keeratan hubungan secara genetik
berukuran 4 x 10 m dengan jarak tanam 60 x 25 cm. antara karakter yang diamati digunakan rumus korelasi
Pengamatan dilakukan pada 100 tanaman contoh setiap sederhana dari SINGH dan CHAUDARY (1977). Di mana
petak. Parameter yang diamati adalah tinggi tanaman pada koefisien genotipik pasangan sifat-sifat adalah sebagai
umur 30, 60 dan 90 HST, umur berbunga, umur panen, berikut :
jumlah cabang per tanaman, jumlah polong per tanaman, kov.fxy
panjang polong, jumlah biji perpolong, berat 1.000 biji dan rfxy =
hasil biji per hektar. (2fx.2fy)0,5
Tetua jantan mempunyai sifat tahan penyakit busuk
pangkal batang, dan ruang polongnya lebih besar. Sedang-
kan tetua betinanya mempunyai sifat produksi tinggi tapi kov.gxy
rentan terhadap penyakit dan ruang polongnya lebih rgxy =
pendek. Variasi genetik untuk semua sifat yang diamati (2gx.2gy)0,5
dihitung dari koefisien keragaman genetik dan koefisien di mana :
keragaman fenotip menurut rumus SINGH dan CHAUDARY rfxy = korelasi fenotip antara sifat x dan sifat y
(1977) sebagai berikut: rgxy = korelasi genetik antara sifat x dan sifat y
kov.fxy = kovarian fenotip antara sifat x dan sifat y
- Keragaman fenotip kov.gxy = kovarian genetik antara sifat x dan sifat y
2f 2yx = ragam fenotip sifat x
KVF = x 100% 2gx = ragam genetik sifatx
X 2yy = ragam fenotip sifat y
2gy = ragam genetik sifaty
- Keragaman genotip
2g Keberhasilan koefisien korelasi di atas dilakukan
KVG = x 100% berdasarkan t-student dari SINGH dan CHAUDARY, (1977)
X sebagai berikut :

89
 JURNAL LITTRI VOL. 13 NO. 3, SEPTEMBER 2007 : 88 - 92

rfxy jumlah cabang per tanaman, dan berat 1.000 biji (Tabel 1),
t= sehingga dapat dikatakan bahwa Koefisien Variasi Genetik
(1-r2 fxy/db)0,5 mempunyai nilai cukup tinggi. Keadaan ini menunjukkan
rgxy bahwa sebagian besar sifat yang diamati dari ketiga
t= persilangan memperlihatkan peluang terhadap usaha-usaha
(1-r2 gxy/db)0,5 perbaikan yang efektif melalui seleksi dengan memberikan
keleluasaan dalam memilih genotip-genotip yang diingin-
di mana : kan, melalui penggalian kombinasi genetik-genetik baru.
rfxy = korelasi fenotip sifat x dan y Selanjutnya RASYAD (1996) mengemukakan bahwa
rgxy = korelasi genetik sifat x dan y nilai koefisien keragaman genetik tinggi, maka faktor
r2 fxy = kuadrat korelasi fenotip sifat x dan sifat y r2 genetik akan berpengaruh besar pada penampilan sifat
gxy = kuadrat korelasi genetik sifat x dan sifat y db tersebut.
= derajat bebas (n-2)
Nilai heritabilitas dalam arti luas untuk sifat tinggi
tanaman dan umur panen dari ketiga persilangan
HASIL DAN PEMBAHASAN mempunyai nilai tinggi. Hal ini berarti bahwa peranan faktor
genetik pada penampilan fenotip sangat besar, atau peranan
lingkungan pada penampilan tersebut kecil. Sedangkan sifat
Pada umumnya nilai Koefisien Variasi Genetik umur berbunga, jumlah cabang per tanaman, jumlah polong
(KVG) menunjukkan kriteria sedang sampai tinggi pada per tanaman, panjang polong, berat 1.000 biji, dan hasil biji
ketiga persilangan, kecuali umur panen dan berat 1.000 biji per tanaman meskipun ada variasi heritabilitasnya dari
pada persilangan Sbr 1 X Si 13, umur panen dan jumlah ketiga persilangan tetapi nilainya masih tinggi karena hanya
cabang per tanaman pada persilangan Sbr 1 X Si 22, satu persilangan yang nilai heritabilitasnya sedang. Ini
sedangkan pada persilangan Sbr 1 X Si 26 nilai Koefisien berarti peranan genetik masih tinggi dan seleksi dapat
Variasi Genetik kecil terdapat pada sifat umur berbunga, dilakukan pada generasi awal.

Tabel 1. Nilai Varians Genetik (2g), Varians Fenotipe (2f), Varians Galat (2e), Koefisien Variabilitas Genetik (KVG), Nilai Heritabilitas (H), dan
Korelasi Genotipik (rg) beberapa sifat penting pada tiga persilangan wijen
Table 1. Values Genetic Variations (2g), Fenotype Variations (2f), Error Variations, Genetic Variability Coefficient (KVG), Heritability Values (H), and
Genotypic correlation of important characteristics of three sesame crosses
Sifat-sifat Genotipe 2g 2f 2e KVG (%) H Rata-rata rg
Hasil biji per
hektar (kg)
Tinggi tanaman G1 111,85 153,86 42,01 6,22 (sedang) 0,73 (tinggi) 169,91 0,98*
(cm) G2 142,15 231,89 89,74 7,29 (sedang) 0,61 (tinggi) 163,65 0,97*
G3 143,39 262,86 199,47 7,63 (sedang) 0,55 (tinggi) 156,88 0,42
Umur berbunga G1 6,90 9,54 2,64 5,85 (sedang) 0,72 (tinggi) 44,92 0,45
(HST) G2 4,36 8,40 4,04 4,91 (kecil) 0,52 (tinggi) 42,50 0,88
G3 1,33 3,18 1,85 2,78 (kecil) 0,42 (sedang) 41,50 -0,01
Umur panen G1 6,19 9,47 3,28 2,58 (kecil) 0,65 (tinggi) 96,33 0,89
(HST) G2 4,36 5,28 1,68 2,03 (kecil) 0,68 (tinggi) 93,50 0,94
G3 2,53 4,92 2,39 1,71 (kecil) 0,51 (tinggi) 93,25 0,09
Jumlah cabang G1 3,64 5,93 2,29 26,46 (besar) 0,61 (tinggi) 7,21 0,99**
per tanaman G2 1,70 4,79 3,09 23,71 (besar) 0,36 (sedang) 5,50 0,99**
(cabang) G3 1,66 2,27 0,61 23,64 (besar) 0,73 (tinggi) 5,45 0,14
Jumlah polong G1 727,98 1002,36 274,38 31,71 (besar) 0,73 (tinggi) 85,09 0,64
per tanaman G2 365,21 616,88 251,67 27,38 (besar) 0,59 (tinggi) 69,80 0,88
(polong) G3 194,16 595,49 401,33 18,08 (besar) 0,33 (sedang) 77,07 0,98*
Panjang polong G1 0,01 0,02 0,01 5,03 (sedang) 0,50 (tinggi) 1,99 0,26
(cm) G2 0,01 0,03 0,02 5,18 (sedang) 0,33 (sedang) 1,93 -0,59
G3 0,01 0,02 0,01 5,03 (sedang) 0,50 (tinggi) 1,99 0,71
Jumlah biji per G1 62,33 232,14 169,81 14,94 (besar) 0,26 (sedang) 52,83 0,98*
polong G2 128,94 282,75 153,81 21,45 (besar) 0,46 (sedang) 52,94 0,95*
(biji) G3 93,64 248,16 154,52 17,59 (besar) 0,38 (sedang) 55,00 0,98*
Berat 1000 biji G1 0,01 0,03 0,02 3,31 (kecil) 0,33 (sedang) 3,02 0,90
(gr) G2 0,03 0,05 0,02 5,57 (sedang) 0,60 (tinggi) 3,11 0,99**
G3 0,01 0,02 0,01 3,13 (kecil) 0,50 (tinggi) 3,19 0,99**
Hasil biji per G1 4426,31 21077,68 16651,37 6,52 (sedang) 0,21 (sedang) 1021,06
hektar G2 6610,96 12242,52 5631,56 8,02 (sedang) 0,54 (tinggi) 1013,83
(kg) G3 12447,74 20077,00 7629,26 9,96 (sedang) 0,62 (tinggi) 1120,03

Keterangan : G1 = persilangan Sbr 1 X Si 13; G2 = persilangan Sbr 1 X Si 22; G3 = persilangan Sbr 1 X Si 26

Note : G1 = crossing Sbr 1 X Si 13; G2 = crossing Sbr 1 X Si 22; G3 = crossing Sbr 1 X Si 26

90
 HANSON (1963) menyatakan nilai heritabilitas dalam
arti luas menunjukkan genetik total dalam kaitannya
keragaman genotip, sedangkan menurut POESPODARSONO
(1988), bahwa makin tinggi nilai heritabilitas satu sifat
makin besar pengaruh genetiknya dibanding lingkungan.
Untuk sifat jumlah biji per polong pada ketiga
persilangan nilai heritabilitasnya sedang. Hal ini menunjuk-
kan bahwa sifat ini tidak dapat digunakan sebagai kriteria
seleksi pada generasi awal, seleksi pada sifat tersebut lebih
baik dilakukan pada generasi lanjut.
Hasil biji per hektar merupakan komponen utama
tanaman wijen yang penting karena bernilai ekonomis. Hasil
biji merupakan sifat yang diwariskan secara kuantitatif dan
dikendalikan oleh banyak gen yang masing-masing mem-
punyai pengaruh sangat kecil.
Dengan demikian seleksi yang ditujukan untuk
perbaikan sifat hasil biji per hektar mempertimbangkan
sifat-sifat yang lain (POESPODARSONO, 1988). Dalam menen-
tukan sifat-sifat yang ada kaitannya dengan sifat yang dituju,
maka diperlukan informasi hubungan antara sifat-sifat
tersebut dengan sifat-sifat yang akan diperbaiki. Hasil
penelitian menunjukkan bahwa korelasi genotipik antara
sifat hasil biji per hektar dengan sifat-sifat yang lain
bervariasi pada ketiga persilangan, di mana korelasi
genotipik berkisar dari – 0,59 sampai 0,99 (Tabel1).
Pada persilangan Sbr 1 X Si 13 terjadi korelasi
genotipik positif nyata pada sifat tinggi tanaman, jumlah
cabang per tanaman, dan jumlah biji per polong. Sedangkan
pada persilangan Sbr 1 X Si 22 terjadi korelasi genotipik
positif nyata antara hasil biji per hektar dengan tinggi
tanaman dan jumlah biji per polong, serta korelasi genotipik
positif sangat nyata dengan jumlah cabang per tanaman dan
berat 1000 biji. Adanya hubungan antar satu sifat atau lebih
sangat baik sebagai indikator untuk memperbaiki suatu sifat
melalui sifat lainnya (PERMADI et al.,1993). Selanjutnya
pada persilangan Sbr 1 X Si 26 terjadi korelasi genotip
positif nyata antara hasil biji per hektar dengan jumlah
polong per tanaman dan jumlah biji per polong, serta
korelasi genotipik positif sangat nyata pada sifat berat 1.000
biji.
Penggunaan kriteria seleksi melalui korelasi sifat
antara hasil biji per hektar dengan sifat penting lain lebih
mantap apabila sifat-sifat yang dikorelasikan tersebut
mempunyai nilai heritabilitas yang tinggi. Pada persilangan
Sbr 1 X Si 13 sifat tinggi tanaman dan jumlah per tanaman
dapat digunakan sebagai kriteria seleksi tidak langsung
untuk meningkatkan hasil biji per hektar, karena selain
mempunyai nilai korelasi genotipik positif nyata juga
mempunyai nilai heritabilitas tinggi. Sedangkan pada
persilangan Sbr 1 X Si 22 sifat tinggi tanaman dan berat
1000 biji dapat digunakan sebagai kriteria seleksi tidak
langsung untuk meningkatkan hasil biji per hektar.
Selanjutnya pada persilangan Sbr 1 X Si 26 sifat berat 1.000
biji dapat digunakan kriteria seleksi tidak langsung untuk
meningkatkan hasil biji per hektar.
KESIMPULAN
Dari hasil penelitian menunjukkan bahwa sifat-sifat
yang diamati pada ketiga persilangan wijen memiliki variasi
genetik yang cukup besar seperti sifat tinggi tanaman,
jumlah buah, jumlah cabang, berat 1.000 biji dan hasil biji
per hektar sehingga memberikan peluang terhadap usaha-
usaha perbaikan genetik melalui seleksi maupun perbaikan
genotip baru.
Untuk seleksi tanaman wijen dari ketiga persilangan
perlu memperhatikan sifat tinggi tanaman dan jumlah
cabang pada persilangan Sbr 1 X Si 13, sifat tinggi tanaman
dan berat 1.000 biji pada persilangan Sbr 1 X Si 22, serta
sifat berat 1.000 biji pada persilangan Sbr 1 X Si 26, karena
sifat-sifat tersebut mempunyai nilai koefisien korelasi
genotipik dengan hasil biji per hektar dan mempunyai nilai
heritabilitas tinggi.
DAFTAR PUSTAKA
ALLARD, R. W., 1960. Principles of Plant Breeding. John
Wiley & Sons, Inc. New York. 485p.
BAHAR, M., dan A. ZEIN, 1993. Parameter genetik pertum-
buhan tanaman, hasil dan komponen hasil jagung.
Zuriat 4(1):4-7.
BPS, 2001. Statistik Perdagangan Luar Negeri Indonesia.
BPS. Jakarta Indonesia.
DESAI, N. D., and S.N. GOYAL, 1981. Major Problems of
Growing Sesame In India and South East Asia. FAO,
Rome, Italy. p.6-14.
ECKEBIL J. P., W. M. ROSS, C. O. GARDNER , and J. W.
MARANVILLE, 1977. Heritability estimates, genetic
correlations, and predicted gains from S1 progeny test
in three grain sorghum Random-mating Populations.
Crop Sci. 17:373-377.
KASNO, A., 1992. Pemuliaan tanaman kacang-kacangan. Hal
39-68 Dalam: Astanto Kasno, Marsum Dahlan,
dan Hasnam (ed). Prosiding Simposium Pemuliaan
Tanaman I. PERIPI. Komda Jawa Timur. p.307-317.
HANSON, W. D. 1963. Heritability. 125-138. In: W.D. Hanson
and H. F. Robinson (ed.) Statistical Genetics and
Plant Breeding. Nat. Acad. Sci., Washington, D.C.
HELYANTO, B., U. SETYO BUDI, A. KARTAMIDJAJA, dan D.
SUNARDI. 2000. Studi parameter genetik hasil serat
dan komponennya pada plasma nutfah rosela. Jurnal
Pertanian Tropika. 8(1):82-87.
PERMADI, C., BAIHAKI, M. H. KARMANA, dan T. WARSA, 1993.
Korelasi sifat komponen hasil terhadap hasil
genotipe-genotipe F1 dan F1 resiprokal lima tetua
kacang hijau dalam persilangan dialel. Zuriat 4 (1):
45-49.
91
POESPODARSONO, S., 1988. Dasar-dasar Ilmu Pemuliaan
Tanaman. PAU-IPB Bekerjasama dengan Lembaga
Sumber Daya Informasi IPB, Bogor. 163p.
RASYAD, A., 1996. Variabilitas genetik dan heritabilitas
karakter agronomis padi lahan pasang surut di
Kabupaten Bengkalis dan Indragiri Hilir. Zuriat 10
(2) : 80-87.
SINGH, R. K., and B. D. CHAUDARY, 1977. Biometrical
Methods In Quantitative Genetics Analysis. Kalyani
Publishers. Indiana New Delhi. 304p.
SUDDIYAM, P. and S. MANEEKHAO, 1997. Sesame (Sesamum
indicum L.). A Guide Book for Field Crops
Production in Thailand. Field Crops Research
Institute. Department of Agriculture. 166 p.
SUPRIJONO, R. MARDJONO, SOENARDI dan N. IBRAHIM. 1994.
Uji Daya Hasil Beberapa Galur Wijen. Laporan Hasil
Penelitian Balittas. p.4-13.
ZEN, S. 1995. Heritabilitas, korelasi genotipik dan fenotipik
karakter padi gogo. Zuriat 6 (1) : 25-31.
5. Lakukan identifikasi isi jurnal dari aspek permasalahan, tujuan dan kesimpulan
yg membahas tema evolusi molekuler/ evolusi genom. Disajikan dalam bentuk
tabel dan disertai artikel aslinya.
Jawab :
Aspek Permasalahan Pada jurnal yang saya identifikasi, jurnal tersebut
meneliti masalah rancangan konsep dari genom
burung zebra finch (Taeniopygia 11.225 ortolog1;1
dari pasangan perbandingan semua DNA dalam ayam
dan burung zebra finch sebagai penyusun urutan
genom. Hal ini terkait dengan 60 hingga 65% dari
jumlah total gen dalam unggas. Menurut jurnal
tersebut rangkaian urutan genom ayam ( Gallus
gallus) merupakan titik awal evolusi pada genom
burung. Selain itu, sifat heterogen dari tingkat
rekombinasi di seluruh kromosom unggas tampaknya
memiliki efek yang signifikan pada evolusi komposisi
basa. Baru-baru ini telah ada upaya untuk
mengidentifikasi gen yang tunduk pada seleksi positif
dalam garis keturunan unggas dan kuantifikasi evolusi
adaptif pada unggas baik berupa gen maupun genom
Tujuan Tujuan dari penelitian pada jurnal tersebut adalah
untuk menganalisis evolusi molekuler pada semua
DNA yang dimiliki oleh ayam dan burung zebra finch
serta genome mamalia. Selain itu juga
membandingkan tingkat urutan divergensi dan evolusi
DNA ayam dan burung zebra finch pada garis
keturunan finch serta di cabang burung leluhur
terkemuka dari perpecahan antara burung dan kadal
beberapa 285 juta tahun yang lalu. Pada penelitian ini
juga mengidentifikasi gen-gen yang dipilih secara
positif dan atau berkembang pesat dalam garis
 keturunan unggas dan menemukan representasi yang
berlebihan dari beberapa kelas fungsional, termasuk
aktivitas pengangkut anion, pengikatan ion kalsium,
adhesi sel dan sitoskeleton mikrotubulus.

Kesimpulan Setelah melakukan analisis komparatif antara dua

unggas genom menggunakan satu kadal dan tiga
spesies mamalia sebagai outgroup. Tingkat pergantian
8384 1: 1 orthologs gen merosot empat kali lipat dan
dikalibrasi dengan catatan fosil. Pada penelitian ini
juga menemukan perbedaan tingkat substitusi yang
jelas antara garis keturunan burung leluhur dan garis
keturunan yang mengarah ke ayam dan burung zebra
finch, dan peneliti berpendapat bahwa perbedaan
mungkin mencerminkan suatu efek dari waktu
generasi. Peneliti menyoroti satu set 58 gen yang
berevolusi di bawah seleksi positif dalam garis
keturunan burung zebra finch pada bagian tertentu di
neurobiologi. Sembilan gen ini juga diekspresikan
secara berbeda dalam inti kontrol vokal yang unik dari
otak burung zebra finch dan mungkin memerlukan
perhatian khusus di masa depan. Akhirnya, hubungan
negatif yang signifikan tetapi rendah antara tingkat
rekombinasi dan ω mendukung prediksi teoritis bahwa
efisiensi seleksi pemurni dapat dikurangi dalam
daerah rendah tingkat rekombinasi.
 Nam et al. Genome Biology 2010, 11:R68
http://genomebiology.com/2010/11/6/R68

RESEARCH Open Access

Molecular evolution of genes in avian genomes

Kiwoong Nam1, Carina Mugal1, Benoit Nabholz1, Holger Schielzeth1, Jochen BW Wolf1, Niclas Backström1,
Axel Künstner1, Christopher N Balakrishnan2, Andreas Heger3, Chris P Ponting3, David F Clayton2 and Hans Ellegren*1

olution in a non-mammalian vertebrate lineage. To analyze basic molecular evolutionary processes during avian evolution, and to contrast these with the situation in
. Weidentified positivelyselectedand/orrapidlyevolvinggenesinavianlineagesandfound an over- representationof severalfunctionalclasses,includinganiontransporteract
e found no evidence that selection for beneficial alleles is more efficient in regions of high recombination; in fact, there was a weak yet significant negative correlation

Background DNA content typically in the range of 1.0 to 1.5 Gb,

There are nearly 10,000 known species of birds and about half to one-third of the amount of DNA found in
many of these have been instrumental in studies of most mammals [5]. It seems clear that this is mainly due
general aspects of behavior, ecology and evolution. Such to a relatively low activity of transposable elements in
basic knowledge on life history and natural history will birds [6]. Second, the avian karyotype is largely
become an important resource for studies aiming at conserved [7] and is characterized by a high degree of
elucidating the genetic background to phenotypic conserved syn- teny. In contrast to mammals, avian
evolution in natu- ral bird populations [1]. There have chromosomes show significant variation in size, with the
already been some attempts in this direction, including karyotype of many species containing five to ten large
the demonstration that the calmodulin pathway is chromosomes ('mac- rochromosomes') that are
involved in the evolution of the spectacular differences comparable in size to small to medium-sized human
in beak morphology among Darwin's finches [2,3] and chromosomes, and a large number of very small
the critical role of MC1R gov- erning variation in chromosomes (<20 Mb) referred to as
plumage color in several bird species [4]. microchromosomes. Third, birds have female heterog-
At the genomic level, birds have attracted the attention amety, with the Z and W sex chromosomes present in
of biologists for several reasons. First, compared to females while males are ZZ. Moreover, and quite
other vertebrates, avian genomes are compact, with surpris- ingly, recent evidence shows that birds do not
estimated have dos- age compensation of Z chromosome genes
[8,9].
* Correspondence: Hans.Ellegren@ebc.uu.se
1 Department
The draft sequence of the chicken (Gallus gallus)
of Evolutionary Biology, Evolutionary Biology Centre, Uppsala genome [10] provided a starting point for evolutionary
University, Norbyvägen 18D, Uppsala, S-752 36, Sweden genomic analyses of birds. For example, it was found
Full list of author information is available at the end of the article
that the rate of synonymous substitution (dS) correlates
nega-
© 2010 Nam et al.; licensee BioMed Central Ltd. This isan open accessarticle distributed undertheterms of the Creative
Commons At- tribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
Nam et al. Genome Biology 2010, 11:R68
http://genomebiology.com/2010/11/6/R68
tively with chromosome size [11], something that may
be related to GC content and recombination rate, which
are both also negatively correlated with chromosome
size. Moreover, the heterogeneous nature of the rate of
recom- bination across avian chromosomes seems to
have a sig- nificant effect on the evolution of base
composition, reinforcing the heterogeneity in GC
content (isochores) [12], which contrasts with the
situation in mammals where isochores are generally
decaying [13]. More recently, there have been initial
attempts toward identify- ing genes subject to positive
selection in avian lineages
[14] and quantification of adaptive evolution in avian
genes and genomes [15].
Now the genome of a second avian species, the zebra
finch (Taeniopygia guttata), has been sequenced and
assembled [16]. With this additional reference point,
comparative genomic analysis of evolutionary processes
in birds can begin in earnest. In this study we analyzed
the molecular evolution of all known single-copy
protein- coding genes shared by the chicken, zebra
finch and
mammalian genomes. We compared rates of sequence
divergence and protein evolution in chicken and zebra
finch lineages as well as in the ancestral bird branch
lead- ing from the split between birds and lizards some
285 million years ago. We looked for signals of
selection to identify interesting genes for functional
studies, similar to previous scans for positively selected
genes in the human genome [17,18].
Additionally, we paid special attention to zebra finch
orthologs of genes that have known significance in
human learning, neurogenesis and neurodegeneration,
using information in the Online Mendelian Inheritance
in Man (OMIM) database. The zebra finch is an
important model organism for these aspects of
neuroscience [19,20]), and indeed this was a major
motivation for the decision to determine its genome
sequence [21]. The zebra finch is a songbird, one of
several thousand oscines in the order Passeriformes.
Songbirds communicate via learned vocalizations, under
the control of a unique cir- cuit of interconnected brain
nuclei that evolved only in
Table1: Summary statistics of theoverall rate of non-synonymous (dN) andsynonymous (dS) substitution, andtheir ratio
(ω) in avianlineages
Pairwise chicken-zebra finch
Overall dN 0.0635
(0.0517-0.0777)
Overall dS 0.4184
(0.3868-0.4584)
Overall ω 0.1517
(0.1270-0.1788)
95% confidence intervals based on resampling are given in parentheses.
Page 2 of
17
songbirds but have parallels in the human brain [22-24].
Studies of vocal learning in songbirds have revealed
roles for lifelong neuronal turnover (neurodegeneration
and neurogeneration) in the adult brain [19,20]. Hence,
it is worthwhile to assess the evolutionary relationships
of genes potentially involved in these processes in both
humans and songbirds.
Results
Pairwise comparison of the chicken and zebra finch
protein-coding gene sets
We identified 11,225 1:1 orthologs from the pairwise
comparison of all protein-coding genes in the chicken
and zebra finch draft genome sequences. This corre-
sponds to 60 to 65% of the total number of genes in the
avian genome [10]. The overall degree of neutral diver-
gence, as approximated by the rate of synonymous
substi- tution (dS) from 1,000 random sets of 150 genes
[25], between these two bird species was 0.418 (95%
confi-
dence interval = 0.387 to 0.458). The overall ω (dN/d
S ) in
the pairwise comparison was 0.152 (95% confidence
interval = 0.127 to 0.179).
Lineage-specific rates of evolution
For most of the subsequent analyses we used codon-
based multiple species alignments of 8,384 1:1 orthologs
of chicken, zebra finch, Anolis (lizard), and three mam-
mals, including platypus, opossum, human or mouse (see
phylogeny in Figure S1 in Additional file 1), thereby
allowing lineage-specific estimates of rates of evolution.
The rationale for focusing on single-copy genes was that
we sought to avoid problems arising from the establish-
ment of orthology/paralogy within gene families of birds
and/or mammals. The estimates are sensitive to proce-
dures for alignment and the substitution rate models
used; see Additional file 2 for a justification of the meth-
ods applied here. Table 1 summarizes the estimates of
mean dN, dS and ω using a free-ratio model for: (i), the
ancestral bird lineage from the split between birds and
lizards some 285 million years ago (MYA) [26] until the
Zebra finch Chicken Ancestral bird lineage
0.0283 0.0239 0.0288
(0.0225-0.0350) (0.0185-0.0316) (0.0241-0.0345)
0.2133 0.1973 0.2600
(0.1929-0.2384) (0.1810-0.2154) (0.2361-0.2834)
0.1326 0.1208 0.1107
(0.1080-0.1601) (0.0973-0.1527) (0.0942-0.1295)
Nam et al. Genome Biology 2010, 11:R68 Page 3 of 17
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spli gur
t e
bet S1
we in
en Ad
the diti
chi ona
cke l
n file
(Ga 1).
lloa dS
nse was
rae) sign
and ifica
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h high
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line zebr
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s, a
for finc
whi h
ch (0.2
we 13)
use than
an in
esti the
mat chic
e of ken
90 line
MY age
A (0.1
[27 97;
]; P <
(ii), 2.2
the ×
chi 10-
cke 16,
n Wil
line cox
age on
; sign
and ed
(iii) rank
, test;
the Tabl
zeb e 1),
ra indi
finc cati
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line diff
age er-
sin enc
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the the
spli mol
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bet ar
we cloc
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Gal
loa thes
nse e
rae two
and para
Ne llel
oav line
es ages
(Fi . dS
of the ancestral genes was 0.
bird lineage significantly P
01 <
was higher correlated 9
(0.260) than in between zebra 2.
fo 2
the two finch and r
terminal chicken on the ×
th 10
branches, basis of 1 Mb e -16,
which is not windows, ze
unexpected explain- ing 13 W
br ilc
given the to 14% of the a
estimated among- ox
fi on
divergence windows nc
times. The variance (Table h sig
divergence at 2). The an ne
four- fold correlations d d
degenerate sites involving the ch ra
showed the ancestral ic nk
same trend, and lineage were ke tes
was highest in weak and non- n, t).
the ancestral significant. re Ju
bird lineage Since local GC sp st
(mean of 1 Mb content is also ec as
inter- vals = conserved ti for
between zebra ve di
0.239), and finch and
higher in zebra ly ve
chicken, ; rg
finch (0.199) controlling for
than in chicken T en
GC content ab ce,
(0.172). We (see Materials le
estimated th
and methods) 2) er
lineage-specific strongly .
mutation rates e
reduced the T wa
by dividing the correlation he
divergence at sa
between zebra ze str
fourfold finch and br
degenerate sites on
chicken a g
with the divergence fin
estimated age co
(from r2 = ch rre
of lineages 0.134 and lin
according to lat
0.141 to r2 = ea io
the divergence 0.024 and ge
times given n
ha be
above. We d
found that the tw
a ee
muta- tion rate si
was lower in n
gn
the ancestral ifi in
bird lineage ca di
(1.23 × 10- ntl vi
9 site-1 year- y du
1)than in both hi al
the chicken gh ω
er va
lineage (1.91 × l-
10-9 ov
er- ue
site-1 year-1; P s
< 2 × 10-16) and all
ω of
the zebra finch 1:
th
lineage (2.21 × an 1
10-9 site-1 year- th ch
1; P < 2 × 10-
e ic
16), and that the
ch ke
rate in the ic n
chicken lineage ke an
was n d
significantly lin ze
lower than the ea br
rate in the ge a
zebra finch (0. fin
lineage (P < 1 13 ch
× 10-5). 3 ort
The ve ho
divergence at rs lo
fourfold us gs
degenerate 0. (r2
sites of 12 =
ortholo- gous 1; 0.
338, P avian genome
< 2 × 10-16). We next
A sought to
correspondin identify genes, Windows based on zebra fi
g analysis for and the Zebra finch/chicken
7,789 human functional
and mouse cate- gories Zebra finch/ancestral
orthologs these genes Chicken/ancestral
(included in are associated
the 8,384 with, that are
genes from candidates for Windows based on the chic
multiple- being involved
with lineage- Chicken/zebra finch
species
alignments) specific Chicken/ancestral
revealed a adaptations
dur- ing avian Zebra finch/ancestral
similarly
strong evolution. We d.f.,
correlation considered the degrees of
(r2 = 0.359, ancestral bird freedom.
P < 2 × 10- lin- eage as
16). well as the
terminal
Moreover, we chicken and
also found a zebra finch
similar lineages
strength of separately, and
correlation in posed three
gene-wise ω specific
val- ues questions.
estimated for First, which
orthologs genes have
from the bird evolved most
lineage rapidly in
(chicken and avian lineages
zebra finch) (high ω
with the values),
mammalian indicative of
lineage either adaptive
(human and evo- lution or
mouse relaxed
lineages; r2 = selective
0.325, P < 2 constraint? For
× 10-16). The this question
gene-wise we used a
correlations likelihood
between ω ratio test to
values for the determine
ancestral bird which genes
lineage had a
(which had significantly
an overall ω higher ω
of 0.110) and value than the
chicken (r2 = mean of all
genes in the
0.178, P < 2 genome.
× 10-16) and These genes
zebra finch are referred to
(r2 = 0.170, as rap- idly
P<2 evolving bird
× 10-16), (REB) genes.
We used this
respectively, approach
were weaker. rather than
simply
Adaptive selecting, for
evolution of example, the
genes in the top 5% or

Table 2: Correlations of divergence

at fourfold degenerate sites
between avian lineages in 1-Mb
windows
Without controlling for GC
Nam et al. Genome Biology 2010, 11:R68
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10% of genes sorted by ω value since the confidence in
ω values is dependent of alignment length and the
number of substitutions within a particular gene.
Second, which genes have evolved more rapidly in
avian lineages than in other amniote lineages (mammals
and lizard)? Here we used a branch model in PAML to
determine which genes had a significantly higher ω in
avian lineages than in other branches of the tree corre-
sponding to our data. These genes are referred to as more
rapidly evolving in birds(MREB).
Third, which genes show evidence of containing
codons that have been subject to positive selection
(referred to as PS genes) during avian evolution? For
this third question we used a branch-site model in
PAML to identify genes containing positively selected
codons with ω higher than 1.
In total, 1,751 genes were identified as evolving
signifi- cantly more rapidly than the genomic average
(REB) in one or more of the three avian lineages (Table
3). Of these REB genes, 203 (12%) were common to all
three lineages (Figure S2 in Additional file 1); 1,649
genes showed evi- dence of more rapid evolution in one
or more bird lin- eages (MREB) than in other amniotes
(Table 3). The great majority (>97%) of these genes
were specific to a single bird lineage, with no gene
common to all three lineages (Figure S2 in Additional
file 1). We also identified 1,886 PS genes in avian
lineages (Table 3). Most (>85%) of these genes showed
evidence of positive selection in only a sin- gle lineage
(Figure S2 in Additional file 1). As for the REB
category, it may contain genes that evolve rapidly due to
positive selection but also due to relaxed constraint.
Using randomization tests, we compared the number of
overlapping genes between the REB and PS gene lists
with the number of overlapping genes from gene lists
generated randomly. For all three avian branches (zebra
finch, chicken, and ancestral bird lineages), the number
of overlapping genes between the PS and REB gene lists
is significantly higher than in randomized data sets (P <
0.001 for all three branches). This shows that the genes
that we identified as rapidly evolving are unlikely to be
dominated by genes evolving under relaxed constraint.
The lists of REB, MREB and PS genes will constitute
a useful resource for future research aimed at finding the
genetic basis of adaptive evolution in birds, in particular
the list of PS genes. Here we provide an initial
character- ization of genes from these lists by first
testing for an
Table 3: The number of REB, MREB and PS genes in different avian lineages
Rapidly evolving bird (REB) genes
More rapidly evolving genes in birds (MREB) than in other amniotes
Positively selected (PS) bird genes
Page 4 of
17
over-representation of specific gene ontologies (Table
4). The term 'cell adhesion' was over-represented among
REB, MREB as well as PS genes in the ancestral bird
lin- eage. Terms related to ion-channel activity were
over-rep- resented among PS genes in both the ancestral
bird and chicken lineages. The ancestral lineage also
showed an over-representation of the terms blood vessel
develop- ment, synapse organization, integrin-mediated
signaling pathway and proteinaceous extracellular
matrix among MREB genes and ofcytokine secretion
among REB genes. In the chicken lineage, telomere
organization and sterol transport were enriched among
REB genes while in the zebra finch lineage microtubule
cytoskeleton was over- represented among MREB genes.
Table S1 in Additional file 1 lists all genes
corresponding to significantly over- represented Gene
Ontology (GO)terms.
If positively selected codons are evenly distributed
across genes and the power to detect such codons is
more or less constant, then the likelihood of detecting
genes containing positively selected codons will
correlate with alignment length. Consistent with this,
three out of three unique overrepresented GO terms
from the list of posi- tively selected genes in the
ancestral bird branch have longer mean alignment length
than genes with other GO terms (P < 0.001, Wilcoxon
rank sum test). However, the overrepresented GO terms
from the list of positively selected genes in the chicken
lineage have actually shorter mean alignment length
than genes with other GO terms, with marginal
significance (P = 0.093). This warrants fur- ther
investigation, from both methodological and biologi- cal
points ofview.
As a comparison, we tested for over-represented GO
terms among positively selected mammalian genes and
genes evolving significantly faster in mammals than in
birds (Table S2 in Additional file 1). However, using the
same criteria as applied to the lists of avian genes, no
GO term was significantly over-represented in the
mamma- lian lists.
Adaptive evolution of neurological genes
The lineage leading to the zebra finch and other
passerine birds is distinguished from the chicken lineage
by major neurobehavioral adaptations that have parallels
in humans, including the evolution of vocal
communication as well as other forms of learning,
memory and social cognition [28]. We filtered the lists
of positivelyselected
Ancestral lineage Chicken lineage Zebra finch lineage
419 1,148 1,202
103 432 1,154
259 883 936
Page 5 of 17

Table 4: Over-represented Gene Ontology terms in REB, MREB and PS genes in avian lineages
Ancestral bird lineage Chicken lineage Zebra finch lineage

Gene Ontologya N b N c Excess P N b N c Excess P N b N c Excess P

1 2 1 2 1 2

Rapidly evolving in birds (REB)

Biological adhesion (B 2) 17 136 2.67 0.013
Cell adhesion (B 3) 17 135 2.69 0.013
Cytokine secretion (B 7) 4 5 17.06 0.013
Telomere organization (B 5) 5 5 7.81 0.024
Telomere maintenance (B 6) 5 5 7.81 0.024
Sterol transport (B 5) 6 7 6.69 0.024
Cholesterol transport (B 6) 6 7 6.69 0.024

More rapidly evolving in birds (MREB) than in other amniotes

Biological adhesion (B 2) 12 136 5.82 0.0002
Cell adhesion (B 3) 12 135 5.86 0.0002
Blood vessel development/maturation (B5) 2 2 65.94 0.061
Synapse organization and biogenesis (B 5) 3 12 16.49 0.088
Nam et al. Genome Biology 2010, 11:R68

Integrin-mediated signaling pathway (B 6) 3 11 17.98 0.088

Proteinaceous extracellular matrix (C 3)
Cytoskeletal part (C 5) 37 124 1.92 0.040
Microtubule cytoskeleton (C 7) 27 83 2.09 0.040
http://genomebiology.com/2010/11/6/R68

Positively selected (PS) in birds

Biological adhesion (B 2) 16 148 3.27 0.016
Cell adhesion (B 3) 16 147 3.29 0.016
Cell-cell adhesion (B 4) 9 57 4.78 0.035
Homophilic cell adhesion (B 5) 5 16 9.45 0.035
Calcium ion binding (M 5) 14 154 2.74 0.035
Anion transmembrane transport activity (M 6) 16 48 3.00 0.006
aB
Terms with a false discovery rate (FDR) of adjusted P < 0.1 are shown. Excess is the fold enrichment for significant Gene Ontology terms. is biological process, M is molecular function and C is
cellular component. The numbers indicate hierarchical level. bNumber of genes in test sample (REB, MREB and PS, respectively). cNumber of genes in reference sample (1:1 orthologs found in the
respective lineage).
Nam et al. Genome Biology 2010, 11:R68
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genes in the zebra finch and chicken lineages to identify
candidate genes likely to contribute to evolution of these
traits. We began by considering the orthologs of genes
that have been most strongly implicated in learning and
neuronal plasticity in humans, identifying them by
searching the OMIM database for all genes associated
with 'learning', 'neurogeneration' or 'neurodegeneration'.
We had data from multispecies alignments for 74, 211
and 107 such genes, respectively (Table 5). We found
that 15, 34 and 23 of these genes (in total, 58 unique
genes) were present in the list of 1,036 genes identified
as posi- tively selected in the zebra finch lineage (Table
5; Table S3 in Additional file 1). For the term
'neurodegeneration' in particular, the number of
positively selected genes is sig- nificantly higher than
expected by chance (P = 0.0076, Fisher's exact test)
given the overall frequency of posi- tively selected
genes among all genes in our study.
We then compared the number of genes classified as
associated with 'learning', 'neurogeneration' or 'neurode-
generation' that were found to be positively selected in
either the chicken or zebra finch lineage (that is, exclud-
ing genes that were positively selected in both lineages).
Interestingly, for each OMIM term the number of
unique positively selected genes was significantly higher
in zebra finch than in chicken (Table 5; 10 versus 5, 27
versus 15, and 16 versus 8, respectively). This indicates
that the songbird lineage has experienced more frequent
adaptive evolution of genes relating to cognitive
functions than the galliform lineage.
The 58 neurological genes evolving under positive
selection in the songbird lineage were further assessed in
two ways. First, we asked whether any of them also
show evidence of accelerated sequence evolution in the
primate lineage, using data from the study of Dorus et
al. [29]. Four genes are present on both lists: ASPM,
GRIN2a, DRD2, and LHX2 (Table 6). Second, we
asked whether any of them are also expressed
differentially within the songbird-specific song control
nuclei of the zebra finch brain. Lovell et al. [30] used a
combination of microarray and in situ hybridization
analyses to identify approxi-
Table5: OMIMsearchfor genesimplicated inneurological processesandthe number of these identified asevolvingunder
positive selection in the chicken and zebra finch lineages
Search term* NOMIM Nalign
Learning 159
Neurogenesis 472
Neurodeg‘eneration 246
*See Materials and methods. 'NOMIM' is the number of human genes identified in OMIM, 'Nalign' is the number NOMIM genes for which we had
data from multispecies alignments. 'PSchicken' and 'PSzebra' are the number of unique positively selected genes found in the chicken and zebra
finch lineages, respectively. P is the significance level in Fisher's exact test comparing the incidence of positively selected genes in chicken
and zebra finch.
Page 6 of
17
mately 300 genes that are differentially expressed in the
song nucleus high vocal centre (HVC) compared to the
underlying brain tissue. We found that 9 of our 58 neuro-
logical genes evolving under positive selection are also
differentially regulated in the high vocal centre (Table 6),
including glutamate receptor ion channel genes.
The relationship between selection and recombination
We sought to elucidate how the intensity of selection
and/or the influence of genetic drift, manifested in ω,
vary across the avian genome. The potential influence of
recombination on ω was of particular interest since the
rate of recombination is unusually heterogeneous within
both the chicken [31] and zebra finch [32] genomes, and
probably so for birds in general. Such heterogeneity
could set the stage for recombination affecting the
efficacy of selection and thereby ω, as predicted by
evolutionary the- ory [33] but for which there is limited
empirical support [34-38].
As a starting point for these analyses we first noted
that there was a weak positive correlation between ω
esti- mated for 1 Mb intervals and chromosome size in
zebra finch (Figure 1; r2 = 0.055, P = 6 × 10-11) and
chicken (r2 = 0.029, P = 3 × 10-6). This confirms similar
observations made for a small set of chicken-turkey
orthologs [11] as well as for chicken-human orthologs
[10], although the effect we detected here with much
larger data sets was considerably weaker than indicated
by those previous studies. There was a strong negative
correlation between the mean divergence of fourfold
degenerate sites of 1 Mb intervals and chromosome size
(Figure 2; r2 = 0.153 in zebra finch and r2 = 0.140 in
chicken, P < 2 × 10-16 in both cases). These correlations
were not limited to the dichot- omy of
macrochromosomes versus microchromosomes (data not
shown); indeed, for many birds chromosome size shows
a relatively continuous distribution without a clear
distinction between macrochromosomes and
microchromosomes [7].
We found a weak yet statistically significant negative
relationship between recombination rate and ω in both
PSchicken PSzebra P
74 5 10 0.050
211 15 27 0.017
107 8 16 0.025
Table 6: Genes implicated in neurobehavioral evolution by converging lines of evidence

Ensembl ID Locus Gene

Evolving rapidly in the primate lineage [29]

ENSTGUG00000000255 DRD2 D(2) dopamine receptor
ENSTGUG00000004249 ASPM Abnormal spindle-like microcephaly-associated
protein
ENSTGUG00000004747 GRIN2A Glutamate [NMDA] receptor subunit epsilon-1
precursor
ENSTGUG00000007079 LHX2 LIM/homeobox protein Lhx2

Differentially expressed in zebra finch song control system [30]

ENSTGUG00000000694 GPR98 G protein-coupled receptor 98 precursor
ENSTGUG00000002176 MCF2 Mcf2 transforming sequence-like
ENSTGUG00000004464 NEFL Neurofilament triplet L protein
ENSTGUG00000005484 GRIA2 Glutamate receptor, ionotropic AMPA 2
ENSTGUG00000006839 CACNA1D Voltage-dependent L-type calcium channel subunit
alpha-1D
ENSTGUG00000007224 PTPRF Protein tyrosine phosphatase receptor type F
ENSTGUG00000007343 RAI1 Retinoic acid-induced protein 1
ENSTGUG00000010757 GRM1 Glutamate receptor, metabotropic 1
ENSTGUG00000015209 SYCP1 Synaptonemal complex protein 1
Neurological genes under positive selection in the zebra finch (see also Table S3 in Additional file 1) were assessed for representation in the
results of two other studies: orthologs under positive selection in the primate lineage (Dorus et al. [29]) and zebra finch genes that are
differentially expressed in song nucleus the high vocal centre compared to the underlying 'shelf' region (Lovell et al. [30]).

zebra finch (Table 7; r2 = 0.030, P = 4 × 10-5) and
chicken (r2 = 0.011, P = 0.005). This could possibly be
related to other factors co-varying with these parameters.
For example, GC is strongly correlated with
recombination rate in both chicken [31] and zebra finch
[32], and in our data GC content correlates negatively
and weakly with ω (zebra finch, r2 = 0.017, P = 0.002;
chicken, r2 = 0.005, P= 0.068). GC content might be
correlated with ω because biased gene conversion tends
to increase ω due to an increased rate of fixation of
slightly deleterious alleles, mimicking adaptive
evolution [39], and higher GC con- tent tends to
decrease the number of synonymous sites [40,41].
Moreover, gene density is higher in avian micro-
chromosomes than in macrochromosomes [10] and there
are strong correlations between chromosome size and
both GC and recombination rate [31]. Gene density
might be critical to the effects of recombination on the
efficacy of selection because more coding sequence
should, in principle, imply more targets for selection.
When we tested for a correlation between recombination
rate and ω at the same time as controlling for GC and
gene density (proportion of coding sequence within 1
Mb windows), we still found weak yet significant
negative relationships (chicken, r2 = 0.006, P = 0.032;
zebra finch,
r2 = 0.008, P = 0.031). The effect is not limited to
regions with very low recombination rate as similar
results were obtained when comparing windows with
zero and non- zero recombination rates (data not
shown).
Discussion
Modern birds form two monophyletic clades, the
Palaeognathae (ratites, like ostrich and its allies) and the
Neognathae (the great majority of contemporary bird
species), which diverged during the cretaceous between
80 and 130 MYA [42-45]. Within the Neognathae, the
first split was between Galloanserae (fowl-like birds
(including chicken), ducks and geese) and Neoaves (>20
different orders) [46,47]. Diversification within Neoaves
seems to have occurred rapidly, with very short internal
nodes in the basal part of the Neoaves tree [45,48]. One
of these early offshoots within Neoaves was the order
Pas- seriformes, to which zebra finch belongs. These
birds typically have small body size and are relatively
short- lived compared to chicken and their allies within
Gal- loanserae.
When judged from the divergence at fourfold degener-
ate sites across more than 8,000 genes, the mean muta-
tion rate in birds was 1.23 to 2.21 × 10-9 site-1 year-1. The
 (a)
0.4
0.3
WW
0.20.2
0.1
0.0
141516171819
log (chromosome size)log (chromosome size)
Figure 1 The relationship between ω estimated for 1 -Mb intervals and chromosome size. (a) Zebra finch; (b) chicken.
rate was lowest in the ancestral bird lineage from the
split between birds and lizards until the split between
Gal- loanserae and Neoaves (1.23 × 10 -9 site-1 year-1),
was intermediate in the chicken lineage (1.91 × 10-9 site-
1 year-
1) and was highest in the zebra finch lineage (2.21 × 10-9
site-1 year-1). This indicates a rate acceleration among
modern birds and particularly so in Neoaves, or more
specifically, in the lineage leading to zebra finch. The
dif- ference in mutation rate between the chicken and
zebra finch lineages is in a direction predicted by a
generation time effect [49]: shorter generation times
among small songbirds may have led to higher per-year
mutation rates. We note that this inference relies on the
underlying assumption of neutrality of fourfold
degenerate sites. To the best of our knowledge there is
no evidence for codon usage bias in avian genes; if it
exists, it seems unlikely that selection for codon usage
on a genome-wide scale would differ among the
investigated lineages to an extent that can explain the
almost twofold higher mutation rate in the zebra finch
compared to the ancestral lineage.
The lower mutation rate estimated for the ancestral
bird branch is sensitive to the accuracy of the estimated
divergence times of birds and lizards (285 MYA), and
of Galloanserae and Neoaves (90 MYA). Previous
molecular datings of the Galloanserae-Neoaves split
have provided estimates in the range of 90 to 126 MYA,
with a mean of
(b)
0.4
0.3
0.1
0.0
141516171819
105 MYA[50]. Using this mean value, instead of 90
MYA, to estimate the substitution rate still leads to a
faster rate in modern birds than in the ancestral bird
branch (zebra finch, 1.90 × 10 -9 site-1 year-1; chicken,
1.63 × 10-9 site-1 year-1; ancestral birds, 1.33 × 10 -9 site-1
year-1). The earli- est divergence estimate of 126 MYA
leads to similar sub- stitution rates in the ancestral and
zebra finch lineages. However, such an old divergence is
not supported by the fossil record, which indicates a
split younger than 100 MYA [42,44]. Importantly, not a
single modern bird is known in the lower cretaceous
(145 to 100 MY) despite a reasonably good fossil record
[43,51,52]. Another poten- tial concern is that, because
of saturation (that is, when multiple substitutions impair
the model to reliably esti- mate substitution rates), the
ancestral branch length may have been underestimated.
It is difficult to directly assess the possible effect of
saturation on the length of the ancestral bird branch.
However, we note that a similar trend (lower rate of
divergence in the ancestral branch) is not evident among
eutherian mammals from the same set of genes (Table
S4 in Additional file 1).
The ancestral lineage from the split between birds and
lizards until the split between Galloanserae and Neoaves
represents, for the most part, dinosaurs that existed
before the appearance of modern birds (Archaeopteryx
fossils date back around 145 MYA). If the estimated
 (a) (b)
0.8 0.8

0.6 0.6

0.4 0.4
Divergence

Divergence
0.2 0.2

0.0 0.0
141516171819 141516171819
log (chromosome size)log (chromosome size)

Figure 2 The relationship between the mean mutation rate (divergence at fourfold degenerate sites) for 1-Mb intervals and chromosome size. (a) Zebra finch; (b) chicken.

mutation rates are correct and if one assumes a genera-
tion time effect, our data would suggest that generation
times in the saurischian dinosaur lineage were typically
longer than in modern birds.
Previous studies of divergence in mammalian
genomes have indicated a low degree of substitution
rate conserva- tion over evolutionary time scales
comparable to that between chicken and zebra finch,
for example, in the

Table7: Bivariateandpartialcorrelations(withGC content andamountof codingsequence controlled for) betweenωand

recombination rate in 1 Mb windows

t d.f. P r2

Zebra finch
Bivariate -4.13 557 0.00004 0.030
Controlled for GC -2.8 556 0.0053 0.014
Controlled for CDS -4.51 556 0.00001 0.035
Controlled for GC and CDS -2.16 555 0.0313 0.008

Chicken
Bivariate -2.82 713 0.0049 0.011
Controlled for GC -2.15 712 0.0320 0.006
Controlled for CDS -2.44 712 0.0149 0.008
Controlled for GC and CDS -2.14 711 0.0329 0.006
CDS, coding sequence; d.f., degrees of freedom; t, t-statistic (t-score) of the slope.
Nam et al. Genome Biology 2010, 11:R68
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comparison between primate and rodent lineages
[53,54]. These estimate have been based on interspersed
repeat elements under the (reasonable) assumption that
these sequences are selectively neutral. Our analysis of
diver- gence at fourfold degenerate sites between
orthologous regions of chicken and zebra finch revealed
a stronger correlation, with 13 to 14% of the variation in
divergence in one lineage explained by variation in
divergence in the other. This could reflect that the
selective constraints on fourfold degenerate sites and
interspersed elements differ (being higher in fourfold
degenerate sites) so that the two approaches are not
directly comparable. Alternatively, there might be
biological explanations for high mutation rate
conservation in birds. When controlling for the local GC
content, the amount of variation in divergence explained
by the orthologous rate is reduced to 2%. This shows
that avian mutation rate conservation is largely
dependent of conservation in base composition. Com-
pared to mammalian genomes, avian GC content is
highly heterogeneous and this heterogeneity has been
maintained during avian evolution [12]. It was suggested
that the heterogeneous recombinational landscape of
birds [12] reinforces GC heterogeneity via biased gene
conversion. Local recombination rates are significantly
correlated between chicken and zebra finch [32] and it
may very well be that there is a causal connection
between conservation in recombination, base composi-
tion and mutation rate[55-57].
Over-represented gene ontologies among positively
selected or rapidly evolving genes
With draft sequences now available for two avian
genomes it is possible to study the role of natural selec-
tion in shaping individual gene sequences during avian
evolution. An impetus for our study was thus to identify
genes and gene categories that have been important for
adaptive character evolution in a vertebrate lineage.
Clearly, there are many morphological, physiological
and behavioral phenotypes that distinguish birds and
mam- mals. A comparative genomic approach has the
potential to contribute towards the identification of the
genetic basis of these differences [58].
Basic characteristics of birds such as feathers, flight
and hollow bones evolved prior to the split of the
chicken and zebra finch lineages. The genetic novelties
underlying these phenotypes should thus have started to
appear in an ancestral lineage. As discussed above, the
ancestral bird branch in the phylogenetic tree formed by
our data corre- sponds mostly to non-avian dinosaurs of
the order Sau- rischia, suborder Theropoda. Genes or
gene categories identified as positively selected or
rapidly evolving in this branch may thus be related to
phenotypic evolution in non-avian dinosaurs rather than
in modern birds. On the
Page 10
of
other hand, many bird-like features may have started to
emerge already for non-avian dinosaurs.
The two GO terms found to be over-represented
among genes evolving under positive selection in the
ancestral bird lineage, calcium ion binding and cell
adhe- sion, largely represent an overlapping set of
genes. Most of these genes (Table S1 in Additional file
1) encode transmembrane cadherins that play a critical
role in cell- cell adhesion in tissue structures. One of
these cadherins, protocadherin-15, is expressed in retina
and we note that another positively selected calcium ion
binding gene, Crumbs homolog 1, is involved with
photoreceptor mor- phogenesis in retina; mutations in
the human ortholog cause retinitis pigmentosa type 12
[59]. The visual ability of birds is superior to other
vertebrates and the molecular adaptations underlying
this phenotype are likely to have been driven by positive
selection.
In the chicken lineage the term anion transmembrane
transporter activity was over-represented among posi-
tively selected genes. The genes annotated with this
term include solute carriers and ion channels involved
with basic cell signaling processes, for example, in
neurotrans- mission. In the zebra finch lineage the term
microtubule cytoskeleton was over-represented among
genes evolving faster in this lineage than in other
branches of the amniote tree. The majority of these are
kinesins and other genes involved with mitosis/meiosis,
sperm motility, cen- trosome formation and
synapsefunction.
It should be stressed that we inferred positive selection
in lineages corresponding to nearly 100 million years or
more of evolution and that large numbers of genes were
uncovered by these analyses. This is likely to reduce the
power of detecting enriched GO terms due to dilution
and failure to capture temporal episodes of adaptive
evo- lution. Moreover, given that our data were defined
by a common set of 1:1 orthologous genes found in
birds, a lizard and mammals, the analysis did not
include lineage- specific genes that may be particularly
responsive to posi- tive selection. These aspects are
probably of relevance to the somewhat surprising
observation that no significantly over-represented GO
terms were found among positively selected or rapidly
evolving mammalian genes. This is seemingly at odds
with previous work in primates that frequently have
revealed categories such as sensory per- ception,
immune defence, apoptosis and spermatogenesis to be
enriched among positively selected genes [17,18,60-
62]. In birds, there have recently been large-scale efforts
toward transcriptome sequencing of several species,
including songbirds [63]. These data will allow study of
the molecular evolution of genes in much shorter
branches of the avian phylogenetic tree than is currently
possible with complete genome sequences, which is
only available for chicken and zebra finch.
Zebrafinchandpositive selectioninneurological genes
The zebra finch communicates through learned vocaliza-
tions ('songs'). Only the male zebra finch produces
learned song, and he learns this song by copying an
adult tutor during a critical period in juvenile
development. Experimental work in zebra finch has
demonstrated the localization and character of neural
circuits involved in developmental song learning and
adult singing [64-67], with dynamic regulation of brain
gene expression in response to singing and song
experience [68-76]. Fifty- eight genes with known roles
in learning, neurogenesis or neurodegeneration in
humans show evidence of positive selection in the zebra
finch lineage. Of these, nine (15%; Table 6) are also
expressed differentially in the song con- trol system,
either at higher or lower levels than in the surrounding
brain tissue, according to the study of Lovell et al. [30].
In comparison, only 2% (390 out of 17,214) unique
brain-derived cDNA probes on that microarray gave
differential hybridization signals in the song control
system. We note that five of the nine genes encode pro-
teins involved in cell surface and synaptic signaling:
volt- age-dependent L-type calcium channel subunit
alpha-1D (CACNA1D), G protein-coupled receptor 98
precursor (GPR98), glutamate receptor, ionotropic
AMPA 2 (GRIA2), glutamate receptor, metabotropic 1
(GRM1), and protein tyrosine phosphatase receptor
type F (PTPRF). GRIA12 is also one of the ion
channel genes that are suppressed in response to song
playbacks as reported in Warren et al. [16].
Four of the 58 genes show evidence of accelerated
evo- lution in the primate lineage: ASPM, GRIN2a,
DRD2, and LHX2. Two of these have apparent roles in
neurogenesis and neuronal development (ASPM and
LHX2). In partic- ular, ASPM (abnormal spindle-like
microcephaly-associ- ated) has been a focus of
speculation with respect to the dramatic evolution of
brain size in humans. Homozygous mutations in ASPM
are a cause of primary microcephaly
[77] and the gene shows evidence of positive selection in
both the human lineage [78-80] and the ancestral lineage
of the apes [81]. Songbirds have also experienced a rela-
tive increase in brain size compared to other avian lin-
eages [82], with the notable emergence of the large and
highly plastic nuclei of the song control system.
However, enthusiasm for ASPM as a key factor in
primate brain evolution has been tempered by findings
that mutations in ASPM are not correlated with
cognitive ability [83,84] and by alternative roles for
ASPM that might place it under selection more broadly,
such as a role in ciliary function [85].
The other two neurological genes that are also acceler-
ated in primates may be considered to have neuromodu-
latory functions that can directly affect learning,
memory and behavior. DRD2 encodes the D2 subtype
of the dop- amine receptor. GRIN2a encodes a
subunit of the N-
methyl-D-aspartate (NMDA) receptor, a subtype of
iono- tropic glutamate-gated ion channel that has well-
estab- lished roles in learning and brain plasticity
(reviewed in [86]). A survey of GRIN2a sequences
across primate spe- cies revealed a specific correlation
between ω and home range size, which is taken to be a
proxy for spatial mem- ory [87]. Spatial memory is well
developed in the song- bird (passerine) lineage and is
especially evident in food- caching species [88], a
behavior that depends on NMDA receptor function [89].
Zebra finches are not studied as a food caching species,
but their nomadic lifestyle implies a highly sophisticated
spatial sense [90]. NMDA receptors have also been
implicated in song learning and song con- trol system
neurophysiology [91,92]. The rich diversity of songbird
species and their adaptations should provide unusual
opportunities for correlating NMDA receptor sequence
evolution with specific behavioral and neuro-
physiological variations.
The strength of selection during avian evolution
The overall strength of selection as manifested in the
genome-wide ratio of non-synonymous to synonymous
substitution rates (ω) was similar in the chicken and
zebra finch lineages (0.12 to 0.13), as well as in the
ancestral bird lineage (0.11). These ratios are about half
that reported among hominids and more similar to what
is seen in the murid and dog lineages [62]. This may be
taken to suggest that the rate of adaptive evolution
and/or the rate of accumulation of slightly deleterious
mutations have been lower in birds than in primates.
However, it is increasingly appreciated that point
estimates of mean ω can be misleading. Mean ω
decreases with branch length and needs to be seen in a
time trajectory framework rather than as a fixed quantity
[93-95]. The apparent lin- eage-specific differences
between hominids on the one side and murids, dogs and
birds on the other may thus simply be accounted for by
branch length. Future research will be needed to explore
how branch length is best accounted for when
comparing mean ω for different lineages. This will be
important when addressing whether life history
variables, such as the effective population size (Ne),
correlate with mean ω. For example, such a correla-
tion might be expected if slightly deleterious mutations
contribute significantly to protein evolution as postulated
by a nearly neutral model [96], giving rise to a negative
relationship between mean ω and Ne [97].
The relationship between natural selection and
recombination in avian genomes
Selection acts in each generation on alleles embedded
within a particular genomic background. Due to recom-
bination, selection will, over time, be able to favor or
dis- favor alleles at individual loci without affecting the
rest of the genome. This comes with a caveat that when
two loci
are genetically linked, selection at one locus will affect
the efficiency of selection at the other: the loci are said
to interfere with each other. Theory predicts that the
strength of interference should be related to the amount
of recombination between the loci; this is the so-called
Hill-Robertson effect [33]. Theoretical predictions on the
consequence of Hill-Robertson interference on coding
sequence evolution depend on the fitness distribution of
segregating variants at non-synonymous sites [98,99]. If
slightly deleterious mutations segregate frequently in the
population, directional selection at one locus will
increase the probability of fixation of such mutations at
linked loci. If beneficial alleles are common in the
popula- tion, the probability of fixation of those
mutations will be reduced at linked loci. These two
scenarios are associated with opposing predictions for
the correlation between recombination rate and ω; in
the former case a negative relationship is expected
whereas in the latter case a posi- tive relationship
isexpected.
The strongest support for Hill-Robertson interference
comes from regions devoid of recombination. For exam-
ple, ω is generally high in the non-recombining sex
chro- mosome, that is, the Y chromosome in systems
with male heterogamety and the W chromosome in
systems with female heterogamety [100-102]. However, it
has been sur- prisingly difficult to find genome-wide
empirical support for Hill-Robertson interference, and
data are currently limited to studies in Drosophila
[34,35,103,104] and a recent study of humans failed to
demonstrate a correla- tion between recombination rate
and ω [37].
It is possible that the power for detecting a
relationship between recombination and ω could be
higher in bird systems because the rate of recombination
is highly het- erogeneous, at least within the two avian
genomes for which detailed information is currently
available on regional recombination rate variation.
Specifically, there is a clear negative relationship
between chromosome size and recombination rate
[10,31] following from an obli- gate recombination
event per chromosomal arm. In chicken, the average
per-chromosome recombination rate ranges from 2
centiMorgans (cM)/Mb up to 10 cM/ Mb [10].
Moreover, there is significant within-chromo- some
variation in the rate of recombination with a strong
'telomere effect'. This is most readily seen in zebra
finch, with rates close to 10 cM/Mb in terminal regions
of the larger (>100 Mb) chromosomes while the central
parts have rates as low as 0.1 cM/Mb; the latter is not
just a 'centromere effect' because these recombination
deserts cover up to 75% of the larger chromosomes
[32].
We do not find support for an increased efficiency of
directional selection in regions of high recombination. If
anything, the data go in the opposite direction since
there was a weak negative, yet significant relationship
between ω and recombination rate in both chicken and
zebra finch
(r2 < 0.01, after controlling for GC content and the
amount of coding sequence); this is the direction pre-
dicted from the hypothesis of an accumulation of
slightly deleterious mutations in regions with low
recombination rate. One obvious explanation for this
weak relationship is that both slightly deleterious and
beneficial variants are common and that their opposing
effects in Hill-Robert- son interference largely cancel
each other out. However, in the absence of simulations
under different distribu- tions of the fitness
consequences of segregation muta- tions this remains an
argument that is difficult to examine.
Another explanation relates to the fact that recombina-
tion rate and ω are measured on very different time
scales. Recombination is recorded from pedigree data
and thus reflects the rate in contemporary populations.
Lineage-specific ω represents substitutions that have
accumulated during, in this case, 90 million years of
avian evolution. If the recombination landscape has
changed frequently during the course of this time period,
this may have weakened the signal of potential
recombination effects on the pattern of efficacy of
selection across the genome. There is limited knowledge
on the evolutionary consistency of regional
recombination rate variation [105]. At a local scale,
recombination hot-spots are ephemeral in the human
genome with little or no evi- dence for hot-spots at
orthologous positions in the chim- panzee genome [106-
108]. As indicated above, recombination rates in birds
are strongly associated with chromosome features, with
highly elevated rates in microchromosomes and in
telomeric regions of larger chromosomes. Given the
high degree of karyotype stabil- ity in birds [7], this may
suggest that the recombination landscape has also
remained relatively stable. Indeed, we have found that
recombination rates in 1-Mb windows of the chicken
and zebra finch genomes to be significantly correlated
[32]. Moreover, the strong correlation observed between
base composition (GC content) and current
recombination rates in both chicken [31] and zebra finch
[32] is consistent with a conserved pattern of
recombination rate variation, at least under the scenario
that recombination drives the long-term evolution of
base composition (maintenance of regions elevated in
GC content) by biased gene conversion [57]. An
alternative possibility is that base composition drives
recombination rate variation and it is conservation of
GC content, or GC-rich motifs [109], that results in the
appearance of recombination rate conservation.
Further, the influence of Hill-Robertson interference
on the accumulation of mildly deleterious substitutions
is not expected to decrease linearly with an increase of
the recombination rate [37,110]. In this context, it is
possible that the recombination rate is too high in most
regions of the chicken and the zebra finch genome to
lead to mea-
surable variation in the efficiency of selection. This
would somewhat contradict the observation of very low
recom- bination rates in the sub-centromeric region of
the larger zebra finch chromosomes [32]. However,
these recombi- nation deserts can have a high effective
number of recombination events given a very large
population size, as is observed for natural zebra finch
populations [111]. In general, it may very well be that
the effective popula- tion sizes of ancestral passerines
have been higher than that of other (larger) birds.
Conclusions
We conducted a comparative analysis between two
avian genomes using one lizard and three mammalian
species as outgroups. Substitution rates were estimated
from 8,384 1:1 orthologs of genes at fourfold
degenerated sites and calibrated with the fossil record.
We found clear sub- stitution rate differences between
the ancestral bird lin- eage and the lineage leading to
chicken and to zebra finch, and argue that the
differences possibly reflect an effect of generation time.
We further report a list of posi- tively selected and/or
rapidly evolving genes in the above- mentioned avian
lineages. GO terms for several
biological processes were over-represented among the
positively selected genes, including anion transporter
activity, calcium ion binding, cell adhesion and microtu-
bule cytoskeleton. We highlight a set of 58 genes
evolving under positive selection in the songbird lineage
that are of particular interest in neurobiology. Nine of
these genes are also differentially expressed in the
unique vocal con- trol nuclei of the songbird brain and
may warrant special attention in the future. Finally, a
significant but low nega- tive relationship between
recombination rate and ω sup- ports the theoretical
prediction that the efficiency of purifying selection may
be reduced in regions of low recombination rate.
Materials and methods
Alignments
We downloaded protein-coding sequences from the
chicken (G. gallus, WASHUC2), zebra finch (T.
guttata, TaeGut3.2.4), green lizard (Anolis
carolinensis, ANOCAR1), short-tailed opossum
(Monodelphisdomes- tica, MonDom5), platypus
(Ornithorhynchus anatinus, OANA5), mouse (Mus
musculus, NCBIM37) andhuman (Homo sapiens,
NCBI36) genome assemblies through biomart [112] in
Ensembl version 55. In order to identify 1:1 orthologs
between zebra finch and each of the other species, we
used a reciprocal Blast best hit approach as implemented
in Inparanoid3.0 [113]. Codon-based pair- wise
alignments from the corresponding protein sequences
were made using MUSCLE3.7 [114]. We used Gblocks
0.91b [115] to eliminate poorly aligned positions. In total,
our analysis was based on 8,384 genes.
Estimates of substitution rates
Pairwise rates
We used the codeml program in the PAML4.1 package
[116] to estimate mean pairwise dS and ω (dN/dS) for all
11,225 1:1 orthologs of chicken and zebra finch from
1,000 concatenated alignments each constructed from
150 randomly chosen genes. Concatenation of align-
ments reduces the sampling variance by producing
longer sequences for which parameters can be estimated
more precisely [25]. The repeated sampling allows
estimation of the within-genome variance (95%
confidence inter- vals).
Fourfold degenerate rate
The neutral lineage-specific substitution rate in 1-Mb
windows of the chicken and zebra finch genomes was
approximated by estimating the divergence of fourfold
degenerate sites (third codon positions of fourfold degen-
erated codons) using a GTR+ Gamma4 model of substi-
tution with the baseml program in the PAML4.1 package.
We based our analysis on windows with at least 1 kb of
degenerate sites.
Lineage-specific substitution rates
We estimated lineage-specific mean d ,Nd , and
S ω using
the free-ratio model [117] in the same way as for the pair-
wise comparison, that is, applying the Heger and Ponting
[25] method. Lineage-specific ω of individual genes was
estimated using the branch model of PAML4.1, making
the branch of interest foreground and collecting ω from
this branch. This method has the advantage that it tends
to show less sampling variance than a free-ratio model.
Mean ω values for 1-Mb windows were estimated by
concatenating all alignments within each window and
using the three-ratio model in codeml. This model was
chosen to reduce the number of parameters and thus to
avoid the problem of over-parameterization when small
numbers of substitutions are analyzed. Windows were
excluded if the alignment length was less than 1 kb or if
the number of substitutions per window was fewer than
200. This approach avoids problems with decreased pre-
cision of estimates (higher sampling variances) when the
number of substitutions is low.
The ω values for individual alignments were calculated
using the three-ratio model in codeml. Alignments were
excluded if dS > 2 or ω > 3 [14]. This analysis was based
on 7,415 genes in birds and on 6,252 in eutherian
mammals.
Statistical models
We used bivariate and partial correlations to analyze the
relationship between ω and recombination rate
separately in chicken and zebra finch. The sex-average
recombina- tion rate for 1-Mb windows was obtained for
chicken from Groenen et al. [31] and for zebra finch
from Back- ström et al. [32]. Partial correlations
controlled for GC content and the amount of coding
sequence within each
 window individually and in combination. Similarly, we
used bivariate and partial correlation (controlling for GC
content) to study the association between divergence at
fourfold degenerate sites from 1-Mb windows in
different bird species. Since the windows were not
identical between zebra finch and chicken, we estimated
the corre- lations separately for zebra finch-chicken, and
for chicken-zebra finch. The similarity in the results
shows that the analysis is not susceptible to the exact
location of windows. When controlling for GC content
in correla- tions between zebra finch/chicken and the
ancestral bird linage, we used the average GC content of
both chicken and zebra finch as an estimate of GC
content in the ancestral lineage.
Identification of candidate genes for adaptive evolution
Rapidly evolving bird (REB) genes
We used a likelihood ratio test to identify genes evolving
significantly faster than the average of all genes in a par-
ticular lineage. To do so, we compared the likelihood of a
model where ω was estimated for a particular gene under
consideration, to a null model where ω was fixed to the
genome-wide estimate of ω (degrees of freedom (d.f.) =
1), followed by multiple testing correction by false discov-
ery rate (q < 0.05) using the program Qvalue [117]. This
gives a list of genes that show significantly different ω
val- ues, both higher and lower, than the genomic average,
of which we considered the genes with higher ω values to
represent faster evolving genes.
Genes more rapidlyevolving in birds(MREB) than in other
amniotes
We used the branch model in codeml to identify genes
that have evolved significantly faster in a particular lin-
eage compared to the rest of the tree. The null hypothesis
assumed that all branches of the tree have the same ω
olving faster in mammals than in other lineages of the amniotes. List of positively selected genes in zebra finch lineage whose human orthologs have been implicated in neurological function (learning, neurogeneration, neu
while the alternative hypothesis allows the tested branch
to have a different ω. We used a likelihood ratio test with
d.f. = 1 to compare the two hypotheses, followed by mul-
tiple testing correction by false discovery rate (q < 0.05)
using Qvalue [117]. This gives a list of genes where ω in
the lineage of interest (zebra finch, chicken or ancestral
bird lineage) is significantly different, either higher or
lower, from ω in the other lineages. We only report the
genes that have significantly higher ω values.
Genes evolving under positive selection
To detect genes containing codons (at least one)
evolving under positive selection in a specific branch
(the fore- ground branch) we used a branch-site test for
positive selection [118,119] implemented in the codeml
program of the PAML4.1 package. We used the
likelihood ratio test 2, with d.f. = 1, with the null
hypothesis that ω2 was fixed to 1 compared to an
alternative model where ω > 1 [120], followed by
multiple testing correction by false dis- covery rate (q <
0.05) using Qvalue [117]. For the analysis
of positively selected genes, alignments with fewer than
45 codons were excluded. This analysis was based on
8,260 genes in birds and 7,690 genes in eutherian mam-
mals.
Gene Ontology analysis
To test for overrepresentation of biological processes,
molecular functions and cellular components among
positively selected or rapidly evolving genes, we per-
formed GO analysis using GoStat [121]. We
downloaded GO annotations for chicken, human and
mouse from Biomart. The analysis was based on Fisher's
exact test between two lists of genes, that is, PS genes
and a refer- ence list of all analyzed genes. Multiple
testing corrected significance values were based on
Benjamini and Hoch- berg [122] correction (adjusted P <
0.1), included with the GoStat software.
Analysis of neurological genes
The OMIM database [123] was searched on 29 March
2009, using three different search phrases and a search
limit set for 'prefix star' (that is, to find only OMIM
terms associated with a known gene sequence). One
search was on the term 'learning'. To search for genes
related to neu- rogenesis, we used this phrase: [(stem
cell AND neur ) OR neurogen ]. To search for genes
related to neurode- generation, we used 'neurogen '.
Human gene IDs in OMIM were cross-referenced and
corrected or com- pleted as needed against the HGNC
database, and used to retrieve Ensembl gene IDs for
human and zebra finch orthologs (Ensembl 53) via
Biomart.
Additional material
Abbreviations
cM: centiMorgan; d.f.: degrees of freedom; GO: Gene Ontology; MREB: more
rapidly evolving in birds; MYA: million years ago; NMDA: N-methyl-D-
aspartate; ω: ratio of non-synonymous divergence over synonymous
divergence; OMIM: Online Mendelian Inheritance in Man; PS: positive
selection; REB: rapidly evolv- ing bird genes.
Authors' contributions
KN carried out the bioinformatic analyses. KN, AH, CPP and BN participated
in the substitution rate analyses. KN, BN and JBWW participated in the
bioinfor- matic analyses of positively selected genes. KN, CM, HS and JBWW
participated in the GO analyses. KN, CNB and DFC participated in the
analyses of the neuro-
logical genes. KN, BN, JBWW and AK participated in the analyses linking
recom- bination rate and efficiency of selection. DFC and HE conceived and
designed the study. KN and HE drafted the manuscript. All authors read and
approved the final manuscript.
Acknowledgements
This work was supported by grants from the Swedish Research Council, the
Knut and Alice Wallenberg Foundation and NIH grant RO1 NS045264. We
thank two reviewers for helpful comments.
Author Details
1Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala
University, Norbyvägen 18D, Uppsala, S-752 36, Sweden, 2Institute for
Genomic Biology, University of Illinois, 601 S. Goodwin Avenue, Urbana, IL
61801, USA and 3MRC Functional Genomics Unit, Department of
Physiology, Anatomy and Genetics, University of Oxford, South Parks
Road, Oxford, OX1 3QX, UK
Received: 30 April 2010 Revised: 18 June 2010
Accepted: 23 June 2010 Published: 23 June 2010
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doi: 10.1186/gb-2010-11-6-r68
Cite this article as: Nam et al., Molecular evolution of genes in avian genomes Genome Biology 2010, 11:R68
6. Buatlah uraian bagaimana mendekatkan evolusi dengan pandangan agama?
Dan bagaimana memanfaatkan konsep dalam evolusi bagi kehidupan kita?
Misalnya konsep seleksi alam, adaptasi untuk survive , rekayasa genetik untuk
benih unggul, dan lain-lain.

Jawab:

Pelaksanaan kloning dewasa merupakan hasil dari penerapan rekayasa

genetika. Hal ini telah berhasil terhadap hewan dan terbukti dengan lahirnya
seekor domba dari proses kloning yang diberi nama Dolly, yang selnya diambil
dari kelenjar susu domba betina dewasa jenis Finn Dorset, sementara sel telur
yang belum dibuahi diambil dari domba betina jenis black Face. Setelah diproses
secara ilmiah, maka lahirlah domba finn Dorset Dolly yang secara genetis identik
dengan domba donor inti sel. Sementara itu proses kloning terhadap manusia
dengan kemajuan dibidang bioteknologi, dimasa depan mungkin berhasil
sebagaimana penelitiannya telah dirintis oleh para peneliti dari Advanced Cell
Technology (ACT) , Massachusetts, Amerika Serikat.

Setelah diteliti menurut hukum Islam, ternyata tidak terdapat keterangan yang
jelas yang mengatur masalah tersebut, hanya di antara para mujtahid tidak
mempersoalkan kloning terhadap hewan, tetapi menurut mereka apabila
diterapkan pada manusia akan menimbulkan masalah, misalnya dalam proses
kloning tanpa membutuhkan sperma laki-laki/suami, tanpa melalui perkawinan,
masalah wali nikah dan lain-lain. Oleh karena itu, ada sebagian ahli hukum Islam
yang memberi fatwa hukumnya haram, dan sebagian para ahli belum
menyampaikan fatwanya, mungkin masih menunggu bagaimana kelanjutan proses
kloning terhadap manusia dimasa yang akan datang. Jadi dalam praktik kloning
terhadap hewan tidak dipermsalahkan oleh agama Islam, namun yang
dipermasalahkan yaitu kloning terhadap manusia.

Keberadan teori evolusi Darwin yang menyatakan bahwa evolusi bersal dari
seleksi alam dapat dibenarkan melalui ilmu pengetahuan, karena teori ini mula-
mula mengungkap misteri asalusul kehidupan manusia secara sistematis dan
filosofis dengan argumen-argumen ilmiah, sehingga teori evolusi dianggap benar
adanya bagi sebagian ilmuan serta dapat dijadikan mitra bagi para ilmuan Islam

dalam mengkaji asal-usul penciptaan manusia yang misterius itu. Namun jika

dilihat dari perspektif Islam, teori evolusi tidaklah diterima kebenarannya,

mengingat Alquran dan hadis secara nyata mengungkapkan penciptaan manusia
pertama “Adam a.s”, dan kelanjutan proses penciptaan manusia setelah itu melalui
keturunan. Dengan demikian, teori evolusi menurut Islam dapat ditolak
keberadaannya, dan hanya dianggap sebagai hipotesis belaka.