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DOI: 10.1111/jbi.

13362

RESEARCH PAPER

Phylogeography and species distribution modelling reveal the


effects of the Pleistocene ice ages on an intertidal limpet
from the south-eastern Pacific

Marıa Cecilia Pardo-Gandarillas1 | Christian M. Ib


an~ ez2 | Felipe I. Torres1 |
Vıctor Sanhueza1 | Alejandra Fabres1 | Joaquın Escobar-Dodero3 |
ndez1
Fernando O. Mardones3 | Marco A. Me

1
Laboratorio de Genetica y Evolucio
n,
Departamento de Ciencias Ecolo gicas, Abstract
Facultad de Ciencias, Universidad de Chile, Aim: The distribution and genetic composition of marine populations is the result of
~ n
Nu ~oa, Santiago, Chile
climatic and oceanographic factors as well as life history strategies. Studying species
2
Departamento de Ecologıa y Biodiversidad,
Facultad de Ciencias de la Vida, Universidad with wide distributions and high dispersal potential in sites that were differentially
Andres Bello, Santiago, Chile
affected during the Pleistocene glaciations provides an opportunity to evaluate the
3
Escuela de Medicina Veterinaria, Facultad
de Ciencias de la Vida, Universidad Andres genetic and distributional effect of glaciations on marine populations, such as the
Bello, Santiago, Chile limpet Siphonaria lesonii. The aim of the present study is to evaluate the differential
Correspondence effects of glaciations on areas covered and not covered by ice sheets during the
Marıa Cecilia Pardo-Gandarillas, Las Pleistocene glaciations.
Palmeras 3425, Nu~ n~oa, Santiago, Chile.
Email: pardogandarillas@gmail.com Location: Intertidal zone of the south-eastern Pacific covering approximately
5,000 km of coastline of Peru and Chile.
Funding information
Fondo Nacional de Desarrollo Cientıfico y Methods: We performed molecular analyses of mitochondrial and nuclear data
gico, Grant/Award Number:
Tecnolo jointly, as well as environmental niche modelling (ENM) of populations of the lim-
3140610, 1130266, 1140540
pet Siphonaria lessonii. Using ENM, we modelled the potential distributional range
Editor: Gustav Paulay of the species in the present and its distribution during the Last Glacial Maximum
(LGM).
Results: Two lineages were found that were separated by a break at 41° S, corre-
sponding to the biogeographical discontinuity previously reported for this region.
Both of these lineages experienced genetic and demographical fluctuations that
match the Pleistocene glaciations; however, the variability was more intense in the
southern lineage. Phylogeography and ENM yielded complementary results for
the southern lineage, which experienced loss of genetic diversity and habitat during
the LGM, whereas the northern lineage evidenced loss of genetic diversity without
distributional changes.
Main conclusions: The phylogeographical and ENM approaches suggest a historical
scenario involving demographic and distributional contractions of S. lessonii surviving
in glacial refugia in the southern portion of the south-eastern Pacific. This study is
the first to include both phylogeographical and ENM analyses of marine species
from the Southern Hemisphere.

Journal of Biogeography. 2018;1–17. wileyonlinelibrary.com/journal/jbi © 2018 John Wiley & Sons Ltd | 1
2 | PARDO-GANDARILLAS ET AL.

KEYWORDS
biogeographical barrier, connectivity, dispersal, environmental niche modelling, glacial cycles,
larval planktotrophic, Last Glacial Maximum, Siphonariidae, south-eastern Pacific, Southern
Hemisphere

1 | INTRODUCTION among populations is influenced by the dispersal potential of marine


organisms (e.g., Haye et al., 2014; Palumbi, 2003). Indeed, it has
The Last Glacial Maximum (LGM), which occurred 19,000– been shown that species with planktotrophic larvae have greater dis-
23,000 years ago (Hulton, Purves, McCulloch, Sugden, & Bentley, persal ability and, in some cases, weaker population structure than
2002), is thought to have had a great impact on the demographic species with direct development (e.g., Kinlan & Gaines, 2003; Marko
and genetic diversity of marine fauna (Fraser, Nikula, Ruzzante, & et al., 2010; Palumbi, 1994; Thorrold et al., 2002). In this way, the
~ez, Iriarte, Ocampo, Iudica, & Cledo
Waters, 2012; Nun n, 2015; occurrence of distinct patterns of connectivity through time could
Wang, Tsang, & Dong, 2015). Contractions and subsequent demo- result in the establishment of different phylogeographical structures
graphic expansions (Expansion–Contraction model, CE, Provan & (Teske et al., 2011) due to fluctuations in demography, diversity, and
Bennett, 2008) have been proposed to explain the displacement and ~ ez et al.,
genetic structure and finally to lineage divergence (Nun
loss of coastal habitat for marine organisms, mainly in species from 2015). In this context, global climate fluctuations have left different
the Northern Hemisphere (e.g., Grant & Bowen, 2006; Hewitt & marks on species depending on larval development (Janko et al.,
Ibrahim, 2001; Kelly & Palumbi, 2010; Larmuseau, Van Houdt, Gue- 2007; Kelly & Palumbi, 2010; Teske et al., 2011).
linckx, Hellemans, & Volckaert, 2009; Marko et al., 2010) but also Southern South America underwent strong climatic fluctuations
for species from the Southern Hemisphere (Ceballos, Lessa, Victorio, during the Pleistocene glaciations due to the formation of ice sheets
& Fernandez, 2012; Fraser, Thiel, Spencer, & Waters, 2010; Macaya (Kaplan et al., 2008; Lomolino, Riddle, Whittaker, & Brown, 2010;
~ ez et al., 2015). This contraction involved a
& Zuccarello, 2010; Nun Rabassa, Coronato, & Martinez, 2011). Along the west coast of
reduction in population size and therefore a deviation from migra- South America, there was an increase in the advection of sub-
tion-drift equilibrium, resulting in a reduction in genetic diversity due Antarctic waters, causing a decrease in sea surface temperatures
to the strengthening of the genetic drift effect when migration or (SST, Hebbeln, Marchant, & Wefer, 2002; Kim, Flato, Boer, & McFar-
gene flow is insufficient to sustain that equilibrium (Freeland, 2005). lane, 2002; Lamy et al., 2004) and global decreases in sea level
In some cases, such as those involving the survival of individuals in (~130 m), which changed oceanographic conditions (Lambeck, Rouby,
glacial refugia, gene flow would have been almost completely Purcell, Sun, & Sambridge, 2014). Recent genetic evidence has shed
blocked, resulting in genetic divergence. However, the exchange of light on the effects of glacial conditions. Specifically, postglacial
propagules during postglacial expansion could have erased the sig- recolonization along the coastline of south-eastern Pacific (Cardenas,
nals of historic isolation (Wang et al., 2015), especially in species Castilla, & Viard, 2009; Fraser et al., 2010; Gonzalez-Wevar et al.,
with high dispersal capacity, which can considerably promote or 2012; Macaya & Zuccarello, 2010; Sanchez, Sepu
 lveda, Brante, &
homogenize the genetic divergence that is created during glacial Cardenas, 2011) and a recent demographic expansion along the
periods (Wang et al., 2015). south-eastern Pacific coast (Cardenas et al., 2009; Haye, Salinas,
In marine environments, the degree of gene flow between popu- ~a, & Poulin, 2010; Iban
Acun ~ ez et al., 2011, 2012) have occurred.
lations within a species (connectivity) is influenced by the type of Furthermore, some species, such as seaweeds (Fraser, Hay, Spencer,
larval development of the species (Haye et al., 2014; Janko et al., & Waters, 2009; Fraser et al., 2010; Macaya & Zuccarello, 2010)
2007; Kelly & Palumbi, 2010; Kyle & Boulding, 2000; Teske, Frone- ~ez et al., 2015; Trovant, Orensanz,
and marine invertebrates (Nun
man, Barker, & McQuaid, 2007). The genetic structure of marine Ruzzante, Stotz, & Basso, 2015), also show phylogeographical breaks
populations reflects interactions among biological features, such as near the southern tip of South America. Despite this, other marine
lifestyle and larval development; contemporary processes, such as invertebrates appear to be genetically homogenous along south-east-
connectivity, that are influenced by oceanographic conditions; and ern Pacific (Cardenas et al., 2009; Gonzalez-Wevar et al., 2012;
historical processes, such as glaciations (Chust et al., 2016; Grosberg Zakas, Binford, Navarrete, & Wares, 2009). Thus, the aforemen-
& Cunningham, 2001; Layton, Martel, & Hebert, 2015; Selkoe et al., tioned findings support the idea that coastal benthic species have
2016). It has been hypothesized that larval development type and its contrasting biogeographical histories that might, in turn, reflect the
duration are the main features that influence the maximum dispersal differential impacts of glaciations (e.g., Gonzalez-Wevar, Sauce
de,
distance of benthic marine species (Haye et al., 2014; Kinlan & Morley, Chown, & Poulin, 2013; Marko et al., 2010; Wares & Cun-
Gaines, 2003; Pelc, Warner, & Gaines, 2009; Selkoe et al., 2016). ningham, 2001). It is also interesting that the effect of glaciations on
Thus, aside from historical climatic changes, larval development type the genetic structure of planktotrophic species is variable. In the
likely affects phylogeographical structure because the connectivity case of Siphonaria lessonii (Blainville, 1827), glaciation was found to
PARDO-GANDARILLAS ET AL. | 3

promote genetic structure, while it had no effect on the genetic biogeographical scale. Here, we analyse the genetic and ecological
structure of Nacella magellanica (Gonzalez-Wevar et al., 2012; Nun
~ez factors influencing its distribution and predict how that distribution
et al., 2015). Theoretically, planktotrophic species should have the has been affected by past climate changes.
highest dispersal and should therefore have higher connectivity. In
contrast, species with direct development are thought to have more
2 | MATERIALS AND METHODS
limited dispersal and lower connectivity between populations (e.g.,
Haye et al., 2014; Kinlan & Gaines, 2003; Palumbi, 1994; Thorrold
2.1 | Sample collection
et al., 2002). Therefore, it is not expected that a deep genetic foot-
print of glaciation would be found for planktotrophic species Samples of S. lessonii were collected from 16 localities distributed
because their high dispersal potential would lead to rapid recovery along the south-western coast of South America from latitude 11° S
following glaciation. to 53° S; the sampling area covered a total of approximately
Phylogeographical studies infer contemporary and historical pro-
cesses from a unique temporal sample of genetic variability (e.g.,
Kelly & Palumbi, 2010; Marko et al., 2010). However, phylogeogra-
phy can be better supported by incorporating spatial information
through the use of environmental niche modelling (ENM). In contrast Venezuela
Guyana
with phylogeographical inference, ENM permits the evaluation of
Colombia
historical changes in the geographical distribution of intraspecific lin-
eages (Hugall, Moritz, Moussalli, & Stanisic, 2002; Peterson, 2001). EQ
Ecuador
Thus, it is possible to evaluate the visual concordance among these
approaches. With ENM, it is possible to estimate the distributional Brazil
range of organisms in the past (Carstens & Richards, 2007) based on
climatic parameters that best explain the presence of individual spe-
cies in the present (Austin, 1987; Peterson, 2001). The spatially 10°S
Ancon Peru
explicit information generated in this way can validate and/or com-
Pucusana
plement biogeographical inferences based on molecular markers
(Carstens & Richards, 2007; Neiva, Assis, Fernandes, Pearson, &
Serr~
ao, 2014). Despite this, phylogeographical studies of marine spe- Arica Bolivia
cies from the Southern Hemisphere have not to our knowledge 20°S Pacific Ocean Iquique
incorporated ENM (Alvarado-Serrano & Knowles, 2014). Paraguay
Chile
The pulmonate limpet Siphonaria lessonii (Blainville, 1824) is an Antofagasta
inhabitant of the rocky intertidal zone of South America in both the
Pacific and Atlantic oceans (Olivier & Penchaszadeh, 1968). In the
30°S
Coquimbo
adult stage, S. lessonii is a benthic species with low mobility; its
Los Vilos Argentina
planktotrophic larvae live approximately seven days (Olivier & Pen-
Punta de Tralca
chaszadeh, 1968). A recent study suggested that the Pacific and Pichilemu
~ ez et al.,
Atlantic populations of this species diverge deeply (Nun Talcahuano
2015). However, that study did not include samples from the Magel-
lan Region of the Pacific, which was directly affected by the Pleis- 40°S Valdivia
Metri
tocene glaciations (Hulton et al., 2002). The aim of the present Ancud Huinay
Quellon
study is to assess the differential effects of glaciations on S. lessonii
populations. Specifically, we will assess these effects in both Pleis- Atlantic Ocean
tocene glaciated and unglaciated areas. With the formation of the
ice sheet and the associated decrease in sea level, some intertidal 50°S
species responded with depth shifts (Fraser et al., 2012). Because as
a pulmonate species S. lessonii must inhabit rocky shores above the
waterline, the only way for it to escape the ice sheet would have
Punta Arenas
been by larval dispersal to ice-free shores. Thus, this species pro-
vides an opportunity to investigate whether larval dispersal influ-
85°W 75°W 65°W
ences population distribution. It is hypothesized that despite having
planktotrophic larvae S. lessonii would show a restricted dispersal F I G U R E 1 Map of the south-eastern Pacific showing sampling
resulting in genetic structuring and limited connectivity that might localities of Siphonaria lessonii. The red circles represent sampling
have finally caused deep phylogeographical breaks on a large localities
4 | PARDO-GANDARILLAS ET AL.

5,000 km of coastline (Figure 1). A total of 561 pulmonate limpets and cropped the extremes of the sequences before including them
were collected (18–40 samples per locality, Table 1) from the upper in the analyses.
intertidal zone during low tide. All samples were fixed in 95% etha-
nol for later molecular analysis.
2.3 | Data analysis

2.2 | DNA extraction, amplification and sequencing 2.3.1 | Genetic diversity


A small piece (~1/2 cm2) of muscle tissue was obtained from each The genetic diversity of the COI and ITS1 genes was characterized
individual and fixed in 95% ethanol for DNA extraction, which was using indexes such as the number of polymorphic sites (S), the num-
later performed using the salting-out method (Aljanabi & Martinez, ber of haplotypes (K), haplotype diversity (Hd), nucleotide diversity
1997). (p) and the average number of pairwise differences between
A 676-base pair (bp) partial sequence of the mitochondrial sequences (Π). These indexes were calculated using ARLEQUIN 3.5.1.3
gene encoding cytochrome oxidase subunit I (COI) and a 640-bp (Excoffier & Lischer, 2010).
partial sequence of the nuclear gene internal transcriber spacer 1
(ITS1) were amplified from the genomic DNA obtained from the
2.3.2 | Intraspecific evolutionary lineages
S. lessonii samples (the method is described in detail in
Appendix S1). The double-stranded PCR products were submitted Distinct evolutionary lineages were identified, and their association
to Macrogen, Inc. for purification and sequencing in both direc- with different regions of the south-eastern Pacific was visualized by
tions using an Automatic Sequencer ABI3730 9 1. The sequences constructing median-joining haplotype networks using the COI and
were edited and aligned visually using PROSEQ 2.9 (Filatov, 2002). ITS1 sequence data; this was implemented in HAPVIEW version Beta
A phylogeographical study of S. lessonii from the Atlantic using (Salzburger, Ewing, & Von Haeseler, 2011).
COI gene (GenBank MG386508–MG386599) has previously been
~ ez et al., 2015). We included data from that publi-
published (Nun
2.3.3 | Genetic structure
cation to make it possible to specifically evaluate whether there is
more than one population unit in southern South America and to The FST and ΦST of the COI and ITS1 genes were calculated in ARLE-
assess the origin (Pacific or Atlantic) of the ancestral population. QUIN using 10,000 permutations to estimate the statistical signifi-
Because the sequences from the Atlantic were shorter (551 bp) cance of the divergence between localities. In these analyses, the p-
than those generated in the present study (676 bp), we aligned values were subjected to Bonferroni correction (Sokal & Rohlf,

T A B L E 1 Genetic diversity of south-eastern Pacific populations of Siphonaria lessonii based on the mtDNA COI/nuclear ITS1 genes.
Localities are arranged by latitude (north to south)
Locality N K S Hd p Π
Ancon 18/17 13/1 25/0 0.94/0.00 0.0067/0.0000 4.529/0.0000
Pucusana 20/22 16/2 24/1 0.97/0.09 0.00589/0.0001 3.984/0.0910
Arica 40/16 31/1 38/0 0.98/0.00 0.0071/0.0000 4.795/0.0000
Iquique 40/16 32/1 40/0 0.98/0.00 0.0073/0.0000 4.938/0.0000
Antofagasta 40/16 30/1 41/0 0.98/0.00 0.0073/0.0000 4.926/0.0000
Coquimbo 39/17 33/1 44/0 0.98/0.00 0.0068/0.0000 4.615/0.0000
Los Vilos 40/16 31/1 44/0 0.98/0.00 0.0084/0.0000 5.704/0.0000
Punta de Tralca 39/16 31/1 44/0 0.98/0.00 0.0088/0.0000 5.949/0.0000
Pichilemu 39/16 33/2 49/4 0.98/0.12 0.0087/0.0008 5.850/0.5000
Talcahuano 36/16 33/1 41/0 0.99/0.00 0.0101/0.0000 6.816/0.0000
Valdivia 38/17 31/1 38/0 0.97/0.00 0.0085/0.0000 5.737/0.0000
Metri 38/16 22/3 34/5 0.86/0.34 0.0075/0.0024 5.038/1.5330
Ancud 36/16 18/1 30/0 0.82/0.00 0.0064/0.0000 4.290/0.0000
Huinay 20/15 14/2 18/5 0.93/0.13 0.0051/0.0011 3.421/0.6670
n
Quello 38/15 21/3 37/4 0.86/0.36 0.0075/0.0019 5.055/0.1810
Punta Arenas 40/16 16/2 15/1 0.70/0.12 0.0014/0.0002 0.937/0.1250
Total 561/263 268/9 135/7 0.97/0.44 0.0110/0.0039 7.422/2.4380

Notes. N: number of specimens sampled; K: number of haplotypes; S: polymorphic sites; Hd: haplotype diversity; p: nucleotide diversity; Π: average
number of nucleotide differences.
PARDO-GANDARILLAS ET AL. | 5

1995). Posterior probability to detect georeferenced genetic struc- short runs. Five independent sets of runs with five replicates were
turing was estimated using the package “Geneland 4.0.2” (Guillot, conducted; each replicate contained one long chain, and 10,000
Leblois, Coulon, & Frantz, 2009; Guillot, Santos, & Estoup, 2008) trees were recorded every 100 increments out of a total of
implemented in R 3.3.1 (R Core Team, 2016). We estimated how 5,000,000 iterations of the MCMC chain using static heating scheme
many clusters (K) or populations there are in the south-eastern Paci- temperatures (1, 1.5, 3.0 and 100,000) and a burn-in of the first
fic (COI and ITS1 gene) and along the South Atlantic coast (including 500,000 iterations. In this way, the Θ and M posterior probability
~ez et al., 2015) using a Monte Carlo Markov
COI data from Nun distributions were generated (Beerli & Palczewski, 2010). Different
chain (MCMC) with 50 million iterations and estimating parameters scenarios of migration direction among n population sizes and n
every 10,000 iterations. These analyses were conducted using mod- (n1) migration rates can be used to detect asymmetric gene flow
els of both uncorrelated frequencies (haplotype frequency vectors (Beerli & Felsenstein, 2001). Moreover, a recent addition to the pro-
mutually independent among populations) and correlated frequen- gramme involves the use of a Bayes factor to determine support for
cies. After the run, the convergence of likelihood scores was different scenarios of migration direction (Beerli & Palczewski, 2010).
checked in TRACER 1.5 (http://tree.bio.ed.ac.uk/software/tracer/) zier-corrected lnML estimates of five
These were calculated from Be
using 10% burn-ins. The model with the greatest log10 of the Bayes scenarios. The first scenario considered northward migration plus
factor (BF, Kass & Raftery, 1995) was chosen in the software TRACER. divergence and later southward migration. The second scenario
involved divergence plus posterior southward migration. The third
included northward migration with later divergence without south-
2.3.4 | Genetic isolation by geographical distance
ward migration, the fourth considered bidirectional (northward and
Isolation by distance was evaluated using only the COI data of this southward) migration, and the fifth included divergence with later
study. Mantel tests (Mantel, 1967) were used to compare the northward migration. Finally, the best migration model was evaluated
genetic distances (FST) and the geographical distances (km) among through a Bayes factor using the thermodynamic approximation of
populations. The one-dimensional model for large distances (ex- marginal likelihoods (Beerli & Palczewski, 2010).
tended habitats) was used. Specifically, we evaluated the linear rela-
tionship between the genetic data and geographical distance,
2.3.6 | Demographical history analyses
y = FST/(1FST) (Rousset, 1997). All tests were performed in ARLE-
QUIN with 10,000 permutations. First, Tajima’s D (Tajima, 1989) and Fu’s FS (Fu, 1997) indices were
calculated in ARLEQUIN. These indices indicate deviations from the
Wright-Fisher mutation-drift equilibrium. Next, using a coalescence
2.3.5 | Number of migrates per generation
framework (Kingman, 1982), a Bayesian Skyline analysis (selected by
The asymmetrical migration rates and population sizes were esti- BF = 1.465 –lnL = 895.97, Drummond, Rambaut, Shapiro, & Pybus,
mated using MCMC in MIGRATE-N 3.2.17 software (Beerli & Pal- 2005) was performed in BEAST 1.8.4 (Drummond, Suchard, Xie, &
czewski, 2010), which allows testing migration between two or more Rambaut, 2012). The posterior distribution of effective population
populations (Beerli, 1998, 2009). The posterior probabilities of size (Ne), together with its respective posterior density interval (at
genealogies were calculated based on the coalescence approach. 95% HPD) and the time to the most recent common ancestor
MIGRATE analysis was performed using the DNA sequence model. (MRCA), were estimated in the coalescence genealogies of the maxi-
Bayesian analysis was utilized to estimate the mutation-scaled popu- mum clade credibility trees (Drummond et al., 2012). For the COI
lation sizes (Θ = Nl, COI gene and Θ = 2Nl, ITS1 gene, with N = ef- sequences, the HKY+I+G model was used as prior (BIC = 10,639.21
fective population size and l = mutation rate) and the mutation- and –lnL = 2,771.77) selected in the software JMODELTEST. Addition-
scaled immigration rate (Μ = m/l, with m = immigration rate). In ally, a relaxed uncorrelated exponential molecular clock model was
these analyses, a 1-year generation time was assumed based on the selected for the analysis by Bayes factor (Table 2), which was per-
lifespan of Siphonaria sirius (Liu, 1994). The mutation rate used in formed in the software TRACER. For the COI gene, the estimated evo-
the present study was 1% per million years (Myr); this rate was lutionary rate of 12.13% substitutions per million years was used in
selected based on fossil data for marine gastropods Cypraeidae and
Polystyra (Meyer, Geller, & Paulay, 2005). The effective number of
migrates per generation (Nm) among populations can be calculated T A B L E 2 Comparison of two molecular clock models for
by multiplying Θ by Μ (Beerli, 1998). The Bayesian analyses were Siphonaria lessonii from the south-eastern Pacific. Bayes factor (BF)
analysis was used to select the molecular clock model with the COI
run using the HKY substitution model as a prior (chosen in the pro-
gene and to perform demographic analyses. UEC: uncorrelated
gramme JMODELTEST, BIC = 9764.27, lnL = 2581.92; Posada, 2008).
exponential clock. The BF is described by Newton and Raftery
A single long chain with slice sampling for the proposal distribution (1994)
was used according to the recommendation of the author (Beerli,
Population Model BF lnP
2013). Short runs were first performed to estimate Θ and Μ from
Northern lineage UEC 25.758 3,207.504
FST and uniform distribution prior for parameters; these were fol-
Southern lineage UEC 0.615 1,861.402
lowed by subsequent runs set using parameters estimated in the
6 | PARDO-GANDARILLAS ET AL.

the demographic analysis (see Appendix S1 and Figure S3.1). A single coefficient; when r was >0.8, only one variable was included as the
chain of 40,000,000 MCMC iterations was employed to perform a potential predictor (Peterson et al., 2011). On the basis of correla-
Bayesian Skyline. Then, 10% of the iterations that had not reached tion analyses (Table S2.1), four independent variables were identified
convergence were burned, and a tree was sampled every 1,000 gen- as candidates for ENM modelling; these were maximum monthly sea
erations. The Bayesian Skyline plots were generated with TRACER. surface salinity (SSS) (biogeo10), annual variance in SSS (biogeo12),
mean annual SST (biogeo13) and annual variance in SST (biogeo17).
Initially, a total of 246 occurrences of S. lessonii in the south-
2.3.7 | Ancestral population reconstruction
eastern Pacific were obtained from fieldwork conducted as part of
To evaluate whether the ancestral population came from the south- the present study (n = 38), from the mollusc collection of the Museo
east Pacific or south Atlantic coasts, a discrete phylogeographical Nacional de Historia Natural, Santiago, Chile (n = 76), from data
analysis using a Bayesian framework was performed using BEAST. In extracted from a scientific literature search (n = 97), and from data
the case of the COI gene, the model HKI+G+I was selected by retrieved from the online collection database of the Global Biodiver-
JMODELTEST for the subsequent Bayesian phylogeographical analysis. sity Information Facility (n = 37) (GBIF, www.gbif.org) (Table S2.2).
~ez et al. (2015). In
In this analysis, we included the COI data of Nun After filtering the occurrence data by removing the duplicated
this way, each limpet was assigned to one of the three regions: the records within a single grid cell and removing occurrences that were
Northern South Pacific (NSP, n = 457), the Southern South Pacific located off the Pacific coast, a total of 179 occurrences remained;
(SSP, n = 134) or the Southern South Atlantic (SSA, n = 62). We these were georeferenced to point locations represented as latitude
modelled each region as a discrete trait using a symmetric substitu- and longitude using the datum WGS84.
tion model, and we reconstructed the ancestral state for all ances- We conducted ENM to determine the potential distribution of S.
tors. We set the clock model for mtDNA COI as an uncorrelated lessonii during the LGM based on estimations of suitable environmen-
relaxed clock with lognormal distribution. We used a coalescent tree  n & Peterson, 2005). Initially, niche models
tal conditions (Sobero
prior with constant population size and a normally distributed prior were calibrated using present-day environmental conditions via MAR-
for the mtDNA clock mean rate of 12.13% substitution per million SPEC layers in MAXENT 3.3.3.k (Phillips, Anderson, & Schapire, 2006).
years, estimated for demographic analyses (Appendix S1), with a To determine the most optimal model configuration, the Akaike infor-
standard deviation of 1.23%. An approximate continuous time Mar- mation criterion (AIC, Burnham, Anderson, & Huyvaert, 2011) was
kov chain rate reference prior was used (Ferreira & Suchard, 2008). used as an evaluation of the models’ predictive capacity to select the
We ran the analysis for 100,000,000 iterations, sampling states best regularization coefficient for posterior analysis. We applied 14
every 10,000 steps. We checked the convergence in TRACER. A maxi- different regularization coefficients ranging from 0.5 to 7 in equal
mum clade credibility tree was obtained using TREE ANNOTATOR 1.8.4. increments and then arranged the AICs corrected by sampled size
(AICc) (Warren & Seifert, 2011). AIC analysis was performed using
ENMTOOLS 1.4.3 (Warren, Glor, & Turelli, 2010). An appropriate regu-
2.3.8 | Environmental niche modelling
larization parameter (i.e., 1) was used for the final contemporary
To identify the potential distribution of S. lessonii in the past and model and for further projections from the past scenario (Table S2.3).
present, we used ENM (Peterson, 2001). This modelling was per- The model was then hindcasted to the LGM environmental data
formed to portray the potential distributional range of the species in selecting the logistic output with 1,000 bootstrap replicates. Extrapo-
the present and during the LGM. The study area for the present-day lation and clamping settings were turned off to prevent inappropriate
and past analyses included approximately 6,000 km of coastline from extrapolation (Owens et al., 2013). Finally, the continuous model out-
Tumbes (3.9° S) to Deception Island (55.8° S). As the geographical puts were used as an expression of the relative suitability of the
dimensions are crucial for ENM (Barve et al., 2011), we generated models based on S. lessonii probability distributions.
30-km (current intertidal zone) and 50-km (LGM intertidal zone) off-
shore buffer masks to delimitate the appropriate habitat. To charac-
3 | RESULTS
terize the present-day conditions, we used 10 ocean bioclimatic
variables, including the annual mean, range, variance and extreme
3.1 | Genetic diversity
values of SST and salinity. The values were retrieved from the Mar-
ine Spatial Ecology (MARSPEC) layers database (Sbrocco & Barber, Among the 561 S. lessonii individuals in which the COI mitochondrial
2013). For ocean paleoclimate conditions (LGM), the same 10 ocean gene was sequenced, 268 haplotypes were found. Most of the 16
bioclimatic variables were gathered from the Paleoclimatic Marine localities sampled exhibited high haplotype diversity, high nucleotide
Spatial Ecology (Paleo-MARSPEC) dataset (Sbrocco, 2014). All the diversity, polymorphic sites and a high average number of nucleotide
environmental data used had 50 spatial resolution. To detect multi- differences between pairs of sequences for individuals from latitudes
collinearity, correlations among pairs of present-day bioclimatic vari- between 18° S and 33° S (Table 1). However, a decreasing trend in
ables were estimated using the Spatial Analysis tool ARCGIS version haplotype diversity was observed, whereas no such trend was evi-
10.3.1 (ESRI, 2015). To reduce model overfitting, the association dent for nucleotide diversity, although Punta Arenas (the southern-
between variables was tested using the Pearson correlation most locality) displayed the lowest values (Table 1). On the other
PARDO-GANDARILLAS ET AL. | 7

hand, nine ITS1 haplotypes were found for the 263 individuals col- the south-east Pacific. The genetic disjunction was found at 41° S
lected throughout the entire distribution range. Overall, the ITS1 in Metri, dividing it between the northern population and the
gene diversity was low and insufficient to estimate connectivity. A southern population (Figure 3a–d). On the other hand, the genetic
single haplotype was found for individuals from almost all northern data of the South Atlantic limpets indicated that they represent
locations. Haplotype and nucleotide was low for most localities, part of the southern population in the South Pacific, forming one
although it increased slightly to the south (Table 1). population unit (Figure 3b). In addition, the Mantel tests based on
COI showed slight but significant genetic isolation by geographical
distance for the northern population or lineage (r = 0.40, p = 0.003;
3.2 | Identification of evolutionary lineages
Figure S3.2).
The COI haplotype network of the evolutionary lineages of S. lesso-
nii was quite ramified and complex (Figure 2a). The haplotypes
3.4 | Number of migrates per generation
were assigned to two distinct lineages, a northern and a southern
lineage (Figure 2a). These two lineages were found to be related to The number of migrates per generation (Θ*M) displayed an asym-
a phylogeographical break and biogeographical disjunction at 41° S metric gene flow; for COI, it was low between the northern and
latitude along the south-eastern Pacific (see map Figure 1). Haplo- southern populations (with COI), with the lowest flow to the south,
types H1 to H206 formed part of the northern lineage, and eleven whereas for ITS1 it was almost symmetrical and residual in both
of these haplotypes (H34, 37, 45, 80, 97, 122, 123, 139, 176, 187 directions. A northward flow and divergence without posterior
and 188) were shared with the southern lineage. In contrast, haplo- southward migration using COI and northward migration plus diver-
types H207 to H268 were found only in the southern lineage, and gence and later southward migration using ITS1 were the migration
almost all were unique or of very low frequency (Figure 2a). The models most strongly supported by Bayes factor analysis (Table 5).
southern lineage comprised the dominant haplotype H122 centrally Under these models, approximately 13.5COI and 0.1ITS1 individuals
linked to 57 other haplotypes separated by up to five mutational per generation were estimated to have migrated in a northward
steps; these formed a star-like network. The ITS1 haplotype net- direction from the southern population (multiply Θ and M, Table 6).
work was simpler than the COI haplotype network (Figure 2b). The In contrast, approximately 1.2COI and 0.3ITS1 individuals per genera-
few haplotypes present in the ITS1 network constituted the same tion were estimated to have migrated from the southern population
two lineages north and south of the biogeographical break at 41° S to the northern population, indicating almost nonexistent migration
latitude. In this network, the dominant H1 haplotype was con- in this direction. Both analyses support a migration model in which
nected by one mutational step to H2 to form the northern lineage. divergence (considering only the data from the North and South
The remaining haplotypes, H4-9, formed the southern lineage (Fig- Pacific) of the two populations occurred approximately 50,000 years
ure 2b). The H1 haplotype was found in 183 specimens from 11 ago (Table 6) during the Upper Pleistocene period (with mitochon-
northern localities, whereas the H4 haplotype was found in 70 drial and nuclear markers).
(69.6%) specimens from five southern localities along the South-
eastern Pacific.
3.5 | Demographic inference
The Tajima’s D and Fu’s FS indices estimated for COI of each of the
3.3 | Assessment of genetic structure and
S. lessonii populations were negative and significant (northern popu-
phylogeographical break
lation: D = 2.02, p = 0.001; FS = 24.67, p = 0.001 and southern
The pairwise FST and ΦST values were low, indicating no significant population: D = 2.14, p = 0.001; FS = 25.77, p = 0.00001). Addi-
differences between Peruvian localities; the values of these parame- tionally, these indices were negative and significant for each locality
ters showed significant differences among the remaining localities that formed part of each population (Table S2.4).
(Tables 3 and 4). The most significant pairwise differences (highest The Bayesian Skyline plot revealed that either populations or
FST and ΦST values for COI and ITS1) were found between the evolutionary lineages of S. lessonii experienced expansions during
localities from Metri to the south and the other northern localities Pleistocene glaciations; these populations or lineages were estimated
(Tables 3 and 4). Thus, the main genetic differences were found to have expanded by one order of magnitude (Figure 4a,b). The Sky-
from Metri at 41° S and southwards, suggesting that there is a line plot of the northern lineage indicated two pulses of demo-
genetic break and phylogeographical divergence at this latitude. The graphic expansion occurring approximately 33,000 and 8,000 years
georeferenced genetic assignment analysis obtained using an uncor- ago (Figure 4a). Additionally, the time to the MRCA for the northern
related frequencies model for the COI gene (chosen by BF = 19.31, lineage was approximately 67,054 years (HDP 95% 53,969–
ln P(model|data) = 2,536.12, SE[] = 1.157) and a correlated fre- 80,402 years, Figure 4a). The southern lineage was estimated to
quencies model for the ITS1 gene (chosen by BF = 3.57, ln P(- have experienced a demographic expansion approximately
model|data) = 60.57, SE[] = 0.102) showed that the 10,000 years ago (Figure 4b). The population likely increased by two
georeferenced genetic data fall with high posterior probabilities orders of magnitude, and the time to the MRCA was likely approxi-
(PP = 0.9) (Figure 3a–d) into two clusters (K = 2) or populations in mately 46,720 years (HDP 95% 38,855–55,727, Figure 4b).
8 | PARDO-GANDARILLAS ET AL.

(a) COI

Northern lineage

(b) ITS1 H2
Northern lineage
H1

H34
H5
H4 H6
H51 H8
Southern lineage
H28 H7
H9
H3

Ancon 5 10 20 40 100
Pucusana
Arica
Iquique
Antofagasta
Coquimbo
Los Vilos
Southern lineage Punta Tralca
H122 Pichilemu
Talcahuano
Valdivia
Metri
H123 Ancud
H188
Huinay
Quellón
5 10 20 40 Punta Arenas

F I G U R E 2 Median-joining networks for Siphonaria lessonii. (a) haplotypes of the mtDNA COI genealogy; (b) haplotypes of the nuclear ITS1
genealogy. Localities are arranged by latitude from north to south

Figure S3.3). In the case of the southern lineage, there was a high
3.6 | Discrete phylogeography analysis
posterior probability that the ancestor inhabited the Southern South
Discrete phylogeography analysis considering the Atlantic data from Pacific (PP = 0.92, Figure S3.3).
~ez et al. (2015) revealed a divergence and almost nearly recipro-
Nun
cal monophyly between the northern and southern lineages approxi-
3.7 | Environmental niche modelling
mately 180,000 years ago (Figure S3.3). The maximum clade
credibility tree shows a higher posterior probability that the most The MAXENT model predicted that the potential distribution of S. les-
ancestral lineage is the North South Pacific lineage (PP = 0.62, sonii changed significantly between the LGM and the present day
PARDO-GANDARILLAS ET AL. | 9

T A B L E 3 FST (below the diagonal) and ΦST (above the diagonal) pairwise comparisons among south-eastern Pacific localities for Siphonaria
lessonii based on COI. The localities are arranged by latitude from north to south
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
1 0.057 0.174 0.182 0.185 0.176 0.158 0.163 0.161 0.176 0.174 0.553 0.606 0.655 0.561 0.822
2 0.020 0.189 0.182 0.178 0.190 0.176 0.176 0.163 0.190 0.213 0.571 0.627 0.677 0.581 0.831
3 0.032 0.017 0.004 0.008 0.004 0.007 0.004 0.000 0.047 0.012 0.509 0.560 0.600 0.518 0.743
4 0.032 0.017 0.000 0.001 0.002 0.009 0.004 0.011 0.038 0.035 0.497 0.549 0.590 0.508 0.734
5 0.034 0.019 0.002 0.004 0.001 0.012 0.001 0.000 0.045 0.020 0.503 0.554 0.594 0.512 0.737
6 0.032 0.017 0.000 0.005 0.000 0.003 0.021 0.002 0.050 0.046 0.514 0.566 0.609 0.525 0.752
7 0.033 0.018 0.002 0.007 0.002 0.005 0.017 0.006 0.011 0.027 0.436 0.490 0.524 0.449 0.683
8 0.032 0.017 0.002 0.004 0.002 0.003 0.004 0.011 0.030 0.004 0.453 0.502 0.536 0.460 0.689
9 0.033 0.019 0.006 0.003 0.000 0.003 0.011 0.009 0.021 0.036 0.457 0.508 0.542 0.469 0.696
10 0.028 0.014 0.003 0.002 0.001 0.003 0.005 0.004 0.004 0.031 0.318 0.373 0.406 0.332 0.586
11 0.037 0.022 0.004 0.013 0.002 0.003 0.003 0.003 0.012 0.007 0.436 0.485 0.523 0.440 0.682
12 0.096 0.081 0.073 0.073 0.073 0.072 0.056 0.074 0.072 0.054 0.069 0.005 0.000 0.012 0.109
13 0.117 0.101 0.091 0.090 0.089 0.088 0.072 0.090 0.088 0.073 0.086 0.004 0.001 0.013 0.073
14 0.058 0.042 0.037 0.037 0.040 0.037 0.029 0.037 0.039 0.018 0.037 0.010 0.040 0.003 0.080
15 0.098 0.082 0.074 0.075 0.077 0.076 0.055 0.076 0.076 0.058 0.071 0.010 0.003 0.012 0.093
16 0.188 0.172 0.156 0.156 0.159 0.157 0.133 0.157 0.158 0.138 0.150 0.012 0.005 0.075 0.010

Notes. Ancon (1), Pucusana (2), Arica (3), Iquique (4), Antofagasta (5), Coquimbo (6), Los Vilos (7), Punta Tralca (8), Pichilemu (9), Talcahuano (10), Valdivia
(11), Metri (12), Ancud (13), Huinay (14), Quello n (15), Punta Arenas (16). The numbers in bold type indicate significant differences among comparisons.
Bonferroni correction level, a = 0.00333.

T A B L E 4 FST (below the diagonal) and ΦST (above the diagonal) pairwise comparisons among south-eastern Pacific localities for Siphonaria
lessonii based on ITS1. The localities are arranged by latitude from north to south
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
1 0.01 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.85 1.00 0.95 0.89 0.98
2 0.012 0.02 0.02 0.02 0.01 0.02 0.02 0.01 0.02 0.01 0.86 0.99 0.95 0.90 0.97
3 0.000 0.015 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.85 1.00 0.95 0.89 0.98
4 0.000 0.015 0.000 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.85 1.00 0.95 0.89 0.98
5 0.000 0.015 0.000 0.000 0.00 0.00 0.00 0.00 0.00 0.00 0.85 1.00 0.95 0.89 0.98
6 0.000 0.012 0.000 0.000 0.000 0.00 0.00 0.00 0.00 0.00 0.85 1.00 0.95 0.89 0.98
7 0.000 0.015 0.000 0.000 0.000 0.000 0.00 0.00 0.00 0.00 0.85 1.00 0.95 0.89 0.98
8 0.000 0.015 0.000 0.000 0.000 0.000 0.000 0.00 0.00 0.00 0.85 1.00 0.95 0.89 0.98
9 0.004 0.025 0.000 0.000 0.000 0.004 0.000 0.000 0.00 0.00 0.78 0.94 0.89 0.82 0.92
10 0.000 0.015 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.00 0.85 1.00 0.95 0.89 0.98
11 0.000 0.012 0.000 0.000 0.000 0.000 0.000 0.000 0.004 0.000 0.85 1.00 0.95 0.89 0.98
12 0.785 0.757 0.779 0.779 0.779 0.785 0.779 0.779 0.717 0.779 0.785 0.12 0.00 0.04 0.06
13 1.000 0.947 1.000 1.000 1.000 1.000 1.000 1.000 0.938 1.000 1.000 0.117 0.00 0.12 0.00
14 0.938 0.892 0.936 0.936 0.936 0.938 0.936 0.936 0.871 0.936 0.938 0.026 0.004 0.00 0.04
15 0.829 0.796 0.824 0.824 0.824 0.829 0.824 0.824 0.760 0.824 0.829 0.005 0.102 0.023 0.04
16 0.939 0.895 0.938 0.938 0.938 0.939 0.938 0.938 0.875 0.938 0.939 0.046 0.000 0.033 0.029

Notes. Ancon (1), Pucusana (2), Arica (3), Iquique (4), Antofagasta (5), Coquimbo (6), Los Vilos (7), Punta Tralca (8), Pichilemu (9), Talcahuano (10), Valdivia
(11), Metri (12), Ancud (13), Huinay (14), Quello n (15), Punta Arenas (16). The numbers in bold type indicate significant differences among comparisons.
Bonferroni correction level a = 0.00333.

(Figure 5a,b). The model predicted that the present-day environmen- the present was uninterrupted north of 41° S; south of this latitude,
tal conditions of the study area in the south-eastern Pacific are mod- suitability was patchy, with some limited areas of higher suitability
erately to highly suitable for S. lessonii. The suitability predicted for (Figure 5a). For the LGM, the model predicted high suitability of
10 | PARDO-GANDARILLAS ET AL.

Map of posterior probability of cluster membership


COI gene ITS1 gene
Northern Population Southern Population Northern Population Southern Population
(a) (b) (c) (d)

Northern
20°S
Population
Northern
Population

Pacific 0.6
30°S Ocean

Latitude
0.5
Latitude

0.3 0.7
0.2
8
0. 3 0.
4
40°S 0.9 .7 0 .4 0.1 0. 0.8 0.9 0.2 0.1
0 0.2 0.8
0.5 0.1 0.9 0.40.7 0.4 0.3
0.6 0.8 0.2 0.6 0.7
0.9
Southern
Atlantic Population
Ocean
50°S
Southern Southern
Population Population

80°W 70°W 60°W 80°W 70°W 60°W 80°W 70°W 70°W


Longitude
F I G U R E 3 Posterior probability maps with assignment of individuals to each genetic cluster of Siphonaria lessonii from the south-eastern
Pacific. Isolines indicate the spatial location of the genetic discontinuity among clusters or populations. Lighter colours indicate higher
probabilities of individuals belonging to that cluster or population. Clusters inferred for (a) the mtDNA COI gene and (b) the nuclear ITS1 gene

T A B L E 5 Comparison of several different migration models for south-eastern Pacific populations of Siphonaria lessonii. Log marginal
likelihoods (Log ML) obtained by Bezier approximation for all models tested. These values were obtained by running the programme MIGRATE-N
several times for appropriate lengths of time. The Bayes factor (BF) calculated from the Bezier approximation, the model choice (MC) and the
model probabilities (MP) using COI and ITS1 genes are shown. Best: Best model
COI ITS1

Model Log ML BF MC MP Log ML BF MC MP


Northward migration—divergence and later southward migration 6,095.3 65.6 1 0.0 961.8 0.0 1Best 0.67
Divergence and later southward migration 6,204.8 284.7 2 0.0 1,023.1 61.2 2 0.0
Northward migration—divergence without southward migration 6,062.5 0.0 3Best 1.0 962.5 0.7 3 0.33
Bidirectional (northward and southward migration) 6,134.1 143.3 4 0.0 979.1 17.2 4 0.0
Divergence with later northward migration 6,190.9 256.8 5 0.0 1,029.2 67.3 5 0.0

Notes. Bayes factors were calculated by subtracting the Bezier-corrected log marginal likelihoods (log ML) of each model. The Bayes factor values were
then used to calculate the exponent values, thereby obtaining the probability values of the models. The model with the highest probability value was
selected as the best model in accordance with the calculated BF following Kass and Raftery (1995), who suggest that values less than 2 do not
deserve mention and that values of 0–2 are positive.

distribution for S. lessonii in the north, and from 35° S southwards value histogram showed differences between the pixel values of the
low suitability values were predicted (Figure 5b). It should be noted present and past distribution models (Figure S3.4). The past model
that the beginning of the unsuitable areas southward of 35° S agrees showed a high percentage of pixels with low probability values,
with the location of the genetic and phylogeographical breaks, which whereas the present model showed a larger percentage of pixels
were mainly detected approximately 41° S (Figure 3). The raster with higher probability values.
PARDO-GANDARILLAS ET AL. | 11

T A B L E 6 Demographic parameters of the two south-eastern Pacific populations of Siphonaria lessonii. The mean values of Theta (Θ) and
immigration rate (M) and their respective (97.5%–2.5%) posterior distribution intervals were estimated under a model of northward migration
with divergence and without posterior southward migration (chosen by Bayes factor). These analyses were estimated using the COI and ITS1
genes
COI ITS1

Population Θ M(?) mean D (northDsouth) Θ M(?) mean D (northDsouth)

Northern 0.093 (0.1–0.0) 50.3 (29.1–6.8) 50.0 (48.1–14.0) 0.00049 297.6 49.9 (45.1–0.0)
Southern 0.024 (0.0–0.0) 145.6 (353.3–0.0) 0.00097 282.6

Notes. Effective population size of northern and southern lineages (Θ); immigration rate per generation (M); divergence event or split from both lineages
(D). The reported values are mean values.

8
10 obtained using both approaches have been reported for marine spe-
(a) Northern Lineage
7 cies of the North Pacific (Bigg, 2014) as well as for species of the
10
North Atlantic (Assis et al., 2015; Neiva et al., 2014). Overall, our
6
10 phylogeographical and niche modelling results are the first reported
results obtained by applying a combination of phylogeographical and
5
10
ENM approaches to a marine species in the Southern Hemisphere.
4
10
Effective Popoulation Size (Ne)

4.1 | Genetic diversity of Siphonaria lessonii


MRCAt

3
10
throughout the south-eastern Pacific coast
2
10
0 10 20 30 40 50 60 70 80 The genetic diversity of S. lessonii displayed a contrasting pattern
8
10 throughout the species’ distribution range along the south-eastern
(b) Southern Lineage Pacific. Very high diversity was detected for the COI mitochondrial
7
10
gene, and lower diversity was found for the ITS1 nuclear gene. For
6 the COI gene, a different haplotype was found for nearly every
10

specimen and locality. In contrast, low genetic diversity was found


5
10
for ITS1; only three alleles were found in total, and specimens of

10
4 most localities had the same allele. Despite this, the low genetic
diversity of ITS1 was sufficient to show a geographical pattern simi-
3
MRCAt

10 ~ ez et al. (2015) found a high


lar to that found for COI. Likewise, Nun

2
diversity of the S. lessonii COI gene for the only two localities sam-
10
0 10 20 30 40 50 60 70 80 pled along the Pacific coast (the northern area in our study). Never-
Time (Thousand Years) theless, because those authors did not sample the Magellan area of

F I G U R E 4 Bayesian Skyline plots showing changes in the the Pacific, we were not able to compare their results with our data
population size over time of Siphonaria lessonii from the south- from the south. Siphonaria lessonii exhibited the same high genetic
eastern Pacific. Effective population sizes were estimated using the diversity as has been found for other planktotrophic Siphonaria from
COI mitochondrial gene of (a) the northern lineage and (b) the Australia (Colgan & Da Costa, 2013; Hodgson, 1999) and South
southern lineage. The time estimates along the x-axis were obtained
Africa (Teske et al., 2011) and higher diversity than the direct devel-
using a calculated substitution rate of 12.13% per million years. The
oper S. nigerrima (Teske et al., 2011). Taken together, the present
effective population size on the y-axis is displayed on a logarithmic
scale. The thick solid lines represent the median estimate of results and those of previous studies reinforce the association
population size; the grey shaded area shows the 95% HPD (highest between planktotrophic larvae, high dispersal potential and high
posterior density) intervals. The bold vertical lines represent the genetic diversity (Chust et al., 2016; Layton et al., 2015; Lee &
median time to the Most Recent Common Ancestor (MRCA); light Boulding, 2009; Selkoe et al., 2016).
vertical lines show the 95% HPD intervals

4.2 | Gene flow and divergent lineages


4 | DISCUSSION
Siphonaria lessonii produces planktotrophic larvae that are capable of
In this study, we evaluate the hypothesis that Pleistocene glaciations remaining in the water column for approximately 1 week (Olivier &
affected the population lineages and demographic pattern together Penchaszadeh, 1968). This feature provides the opportunity for the
with the geographical distribution of the pulmonate limpet S. lessonii species to disperse long distances, maintaining genetic homogeneity.
using both phylogeography and ENM approaches. Similar results Indeed, the genetic isolation by distance found for the northern
12 | PARDO-GANDARILLAS ET AL.


Ecuador
(a) Present (b) Past
5°S

10°S Peru Brazil

15°S
Bolivia
20°S

Chile Paraguay
25°S
Pacific
Latitude

Ocean
30°S
Uruguay Probability distribution
35°S Present Past
Argentina
0.14 0.12
0.25 0.24
40°S 0.36 0.35
0.47 0.47
0.57 0.59
45°S Atlantic 0.71
0.68
Ocean 0.79 0.83
0.89 0.95
50°S
Genetic Break

55°S 0 500
Km

80°W 70°W 60°W 80°W 70°W 60°W 50°W 40°W


Longitude
F I G U R E 5 Environmental niche modelling of Siphonaria lessonii estimated using MAXENT. Potential distributional range was estimated for
present-day conditions (a) and for the Last Glacial Maximum (b). Red and yellow colours denote the highest and lowest probabilities,
respectively, of a suitable environment. The black horizontal line indicates the latitude at which the genetic break was found in the genetic
structure analyses

lineage suggests that long-range dispersal maintains genetic cohesion exceed the tolerance limits of many species (Camus, 2001; Iban
~ ez,
up to distances of approximately 2,000 km (Figure S3.2). In addition, Camus, & Rocha, 2009). Other examples of phylogeographical breaks
the genetic differentiation found in the present study was present at this latitude have also been reported in other marine organisms,
mainly among the most distant areas of the south-eastern Pacific such as molluscs and barnacles (Ewers-Saucedo et al., 2016; Sanchez
coast (Tables 3 and 4). Despite the evidence that S. lessonii is cap- et al., 2011). This break drove the divergence of the northern and
able of long-range dispersal and that connectivity is maintained at southern lineages of S. lessonii, which are nearly reciprocally mono-
large distances, the finding of a genetic break and phylogeographical phyletic (Figure S3.3). The northern lineage includes mostly individu-
divergence at 41° S indicates that this limpet is not able to over- als from the NSP, while the southern lineage comprises individuals
 Island
come contemporary dispersal barriers present around Chiloe from the SSP and also from the SSA (Figure S3.3). In this context,
(between 41–42° S, Camus, 2001). The phylogeographical diver- ~ez et al. (2015), although without studying samples from the
Nun
gence that occurred during the Pleistocene is reinforced at the pre- southern Pacific, also found two lineages, one from the central Chi-
sent time by this biogeographical discontinuity. The austral region lean province and one from the Magellan-Argentinean Province (in
where the break is found is formed by fjords and channels that exhi- their study, these were designated LI and LII, respectively), and sug-
bit important shore-coast gradients in salinity and SST that may gest a recent migration from the ancestral Pacific lineage to the
PARDO-GANDARILLAS ET AL. | 13

Atlantic. In the present study, we corroborate this evolutionary sce- demographic expansion; therefore, it was not included in this analy-
nario, in which the most ancestral lineage inhabited the northern sis. These results are consistent with the known glaciogenic history
South Pacific; by divergence, the ancestral lineage then gave origin of the LG in southern South America (Clapperton, 1993, 2000). The
to the southern lineage in the southern South Pacific approximately glacigenic deposits of the LG were formed during the Upper Pleis-
180,000 years ago (Figure S3.3). This southern lineage then likely tocene (85,000 years ago). This was associated with the slow forma-
gave rise to the youngest lineage from the southern South Atlantic tion of the Patagonian Andes mountain ice sheet reaching up to the
approximately 25,000 years ago (Figure S3.3). In its southern lineage, coast, which occurred at least 30,000 years ago (Rabassa, Coronato,
the limpet exhibits long-range dispersal capacity, maintaining its & Salemme, 2005; Rabassa et al., 2011). Our results suggest that the
genetic cohesion over long distances between the Pacific and Atlan- first expansion pulse of the northern lineage during this period (Fig-
tic coasts in a way that is probably facilitated by the marine currents ure 4a) took place during the glacial recession that occurred 50,000–
system, as has been evidenced in previous studies (Ceballos et al., 25,000 years ago (Laugenie, 1984; Rabassa et al., 2005). This was
2012; Trovant et al., 2015). However, evidence also suggests that followed by a slower and more gradual demographic expansion
some species with planktonic stages share genetic structure between 25,000–15,000 years ago (Figure 4a); the latter expansion was con-
the Pacific and Atlantic coasts (Gonzalez-Wevar et al., 2012). cordant with readvances of the ice sheet that took place 25,000–
17,000 years ago during the LGM. A similar scenario has been
demonstrated in other molluscs (Marko et al., 2010). Finally, a sec-
4.3 | Demographic history
ond expansion pulse occurred approximately 8 ka, causing the popu-
The evidence for excesses and deficits of alleles in the northern and lation to increase by two orders of magnitude. The second
southern lineages, respectively, (Figure 2a,b) is suggestive of demo- expansion coincided with the beginning of the Holocene interglacial
graphic fluctuations (Fu, 1997). Together with the demographic period (Rabassa et al., 2011). As corroborated by the ENM of the
reconstruction and ENM, these results support the idea that the two LGM (Figure 5b), this demographic contraction, which was associ-
lineages experienced historical population expansion, although this ated with loss of genetic diversity, was not associated with shrinkage
expansion occurred in different ways. A possible scenario is that the of the northern end of the distribution range (Figure 5b). Instead,
ancestral lineage may have been distributed throughout the south- the model suggests that the habitat north of 35° S was and currently
eastern Pacific during an interglacial period and that it subsequently is highly suitable for this species (Figure 5a,b). The niche modelling
experienced divergence 180,000 years ago during a glacial period results indicate that there were no local extinctions (i.e., habitat loss)
(Figure S3.3). According to the two migration models (COI and ITS1, that restricted the distribution range in the northern part of the dis-
Table 6), which also support a deep divergence between the two lin- tribution (Figure 5a,b), although oceanographic and climate fluctua-
eages (although more recently estimated, since data for COI in the tions likely affected the demography of this species during the LGM
Atlantic were lacking), reduced gene flow led this divergence and (Hebbeln et al., 2002).
produced a gradual genetic and phylogeographical separation of the According to the expansion-contraction model (Provan & Ben-
two lineages during the Last Glaciation (LG, Rabassa et al., 2011). nett, 2008), the typical star-like genealogy and demographic infer-
During the LG, a series of glacial-interglacial cycles took place that ence of the southern lineage indicates a sudden expansion
affected the phylogeographical patterns of this limpet more than (Figures 2a,b and 4b). A demographic response of this type has also
once. Certainly, other mollusc species have also experienced post- been proposed for other species in southern South America (Cebal-
glacial demographic expansions in northern (Pardo-Gandarillas, los et al., 2012; Gonzalez-Wevar et al., 2012; Nun
~ez, Gonzalez, &
Ib
an~ez, Yamashiro, Me
ndez, & Poulin, 2018) and southern South rez-Losada, 2010). The modelled ice sheet for southern South
Pe
America (Cardenas et al., 2009; Gonzalez-Wevar et al., 2012; America would have reached the continental shelf south of 43° S
Macaya & Zuccarello, 2010). Overall, the formation of the ice sheet (Hulton et al., 2002), implying habitat loss (local extinctions) for S.
during the glacial cycles had a strong and widespread effect that lessonii in this region. This would have caused the southern lineage
resulted in the demographic contraction of S. lessonii populations. It of S. lessonii to have experienced a strong contraction of its effec-
is apparent that the strongest effects of this contraction would have tive population size, genetic diversity, and distribution range during
been in the south, where individuals could only have survived in the LGM. However, the species likely survived in refugia in the
refugia, as has been found for other marine taxa (Gonzalez-Wevar, south during the LGM (Figure 5b), where this lineage would have
~ ete, & Poulin, 2011; Montecinos et al., 2012). This, in
Nakano, Can generated new genetic diversity (Figure 2a,b). These novel and
turn, would have made subsequent migration impossible and rein- unique haplotypes would have been generated approximately
forced the deep divergence between the two lineages (Figure S3.3). 10,000 years ago, coinciding with the beginning of the last glacial
The northern lineage networks indicated by both markers (Fig- recession during the lower Holocene (Rabassa et al., 2011). ENM
ure 2a,b) and demographic inference (Figure 4a) suggest that S. les- indicated that the area south of 41° S supports a highly suitable
sonii experienced repeated population size contractions and loss of distribution at present (Figures 5a and S3.4) but that this area had
genetic diversity since approximately 70,000–80,000 years ago. It low suitability during the LGM (Figures 5b and S3.4). All in all, this
must be noted that the ITS1 gene is less variable than the COI gene translates to a loss of habitat, with few isolated areas serving as
and would require more time to provide evidence of a signal of refugia (Figure 5a,b).
14 | PARDO-GANDARILLAS ET AL.

Lastly, despite the species’ larval dispersal potential, a deep phy- ORCID
logeographical divergence of S. lessonii was found to have occurred
Marıa Cecilia Pardo-Gandarillas http://orcid.org/0000-0003-2626-
as a consequence of climate fluctuations during the late Pleistocene.
8243
This shows that in this species dispersal has been insufficient to
n
Christian M. Iba ~ez http://orcid.org/0000-0002-7390-2617
homogenize the genetic divergence created by glacial periods,
namely the biogeographical break at 41° S. In brief, the biogeogra-
phy of this limpet differed for the two lineages. There was evidence
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