Anda di halaman 1dari 4

Behavioral Ecology Vol. 15 No. 3: 520523 DOI: 10.

1093/beheco/arh039

The origin of parental care in birds: a reassessment


Tomasz Wesoowski Department of Avian Ecology, Wrocaw University, 50 335 Wrocaw, Sienkiewicza 21, Poland
irds reproductive biology is unique in several respects, including patterns of parental care. Biparental care is the norm in birds; it occurs in more than 90% of living species (Kendeigh, 1952), whereas in all other animal groups, if biparental care occurs at all, it is much less common than is uniparental paternal or maternal care (Clutton-Brock, 1991). The reasons for this peculiar pattern are still not fully understood. The studies on avian parental care usually assumed that biparental care was primitive in birds, and theoretical effort was concentrated on nding ways to explain how unaided male or female care could have evolved from it (references in Wesoowski, 1994). The problem of how this avian biparental care system has evolved in the rst place was usually completely ignored. Fortunately this situation has been changing lately. Several studies pursued problems of the evolutionary origins of parental care by attempting to reconstruct the earliest stages of parental care in birds. The rst serious attempt to derive parental care origins from the reptilian state was made by Kavanau (1987). He proposed that the appearance of parental care and further changes in its mode in stem reptiles constituted the rst major event in avian evolution. In other words, the rst step on the way leading to birds was the achievement of advanced biparental care (consisting of egg guarding, as well as grooming, protecting, and escorting of young) by stem reptiles. All other changes, such as attaining homeothermy and the ability to y, came later. So the rst birds would have been biparental with precocial young. Kavanau also proposed that the main force behind the evolution of ight was the need in arboreal reptiles to gain rapid access to ground nests. Van Rhijn (1984, 1990), Elz _ anowski (1985), and Handford and Mares (1985) were the rst to suggest that the earliest form of parental care in birds was unaided male care derived from lack of care in the reptilian ancestors. Following their arguments and other sources of information, I proposed a multistage model of the origin of parental care and the evolution of parental roles in birds (Wesoowski, 1994) as an alternative to Kavanaus scenario. It assumed that powered ight evolved for reasons independent of reproduction, and that parental care evolved as a response to it, within a framework of limitations set by adaptations to aerial locomotion. The unique system of care was then explained in terms of evolutionary responses to the design constraints created by, and ecological opportunities associated with, the origin of ight. It was proposed that evolution proceeded initially through stages without parental care (main adaptations to ight appeared then) but with increasing investment in eggs, resulting in the appearance of sequential ovulation and of very large eggs, thus producing young able to y shortly after hatching. It was suggested that parental care appeared only at that stage, and that it was unaided paternal care (preserved in some groups). Biparental care then evolved from unaided male care. This model was corroborated and extended by Ligon (1999). Moreover, results of an analysis of incubation patterns in extant birds by Vehrencamp (2000) also suggested that the ancestral state for birds was sole male

incubation, from which several forms of shared incubation and female only care have arisen. However, several investigators (Burley and Johnson, 2002; Prum, 2002; Tullberg et al., 2002; Varricchio et al., 1999) have recently challenged the no care to male care rst hypothesis and proposed that parental care is primitive in Archosuaria. They proposeanalogously to Kavanaus (1987) modelthat changes in the mode of parental care in some ordinary reptiles constituted the rst major event in avian evolution; that is, the rst step along the way leading to birds was the achievement of advanced biparental care (consisting of egg guarding, incubation, as well as protecting and escorting of young) by reptiles. The ability to y came later, without a tight relationship to the parental care mode. Tullberg et al. (2002) and Burley and Johnson (2002) claim to reject the male care rst scenarios, and the latter investigators write, Arguments for the male care rst hypothesis have not been presented in any detail. . ., and thus they cannot be inspected closely. . . Proponents of the male care rst hypothesis need to articulate scenarios that would obviate these problems. Being one of them, I feel called to the blackboard. I begin these comments by addressing the strength and validity of the main paleontological, phylogenetic, and cost/ benet arguments put forward in favor of the maternal care rst scenarios. I conclude by proposing a set of minimum requirements that any comprehensive theory of the origin of parental care should fulll. As not all investigators using terms such as parental care, incubation, or (in a paleontological context) even bird or avian mean the same, it is necessary to dene these terms to avoid ambiguities. In the present discussion, parental care will be limited to behavioral aspects of the enhancement of egg and/or young survival by parents, taking place in the postoviposition period (Wesoowski, 1994); bird or avian, to the rst organisms capable of powered ight and all of their ancestors; and incubation to direct transfer of heat from parents body to eggs. Have dinosaurs incubated? In a recent review, Prum (2002) writes, It is little appreciated that fundamental aspects of avian reproductive biology evolved during early archosaurian and theropod ancestry. It is easy to see, however, that extensive parental care is primitive to archosaurs. What is the justication for these statements? Norell et al. (1995) described from Upper Cretaceous deposits of Mongolia an Oviraptor specimen fossilized on top of a nest with eggs. They suggest that this individuals proximity to the nest was related to parental care and conclude that this nding provides the strongest evidence yet that modern avian brooding behavior evolved long before the origin of modern birds and among non-avian maniraptoran theropods. Varricchio et al. (1997) describe two nests of Troodon formosus from Late Cretaceous deposits in Montana containing partially buried eggs. One of them contained 22 eggs, bottom parts of which formed a paired arrangement.

Downloaded from http://beheco.oxfordjournals.org/ by guest on April 23, 2013

Behavioral Ecology vol. 15 no. 3 International Society for Behavioral Ecology 2004; all rights reserved.

Wesoowski

Origin of parental care in birds

521

This pattern, though, was not visible in the second clutch composed of 24 eggs, in which the eggs were tightly packed (their bottom parts were not visible). They use these observations and that of a nest structure, to conjecture that (1) eggs were laid two at a time at one- to several-day intervals, so a lengthy laying period was necessary to complete a clutch; (2) eggs were incubated by direct body contact; and (3) the same was true for Oviraptor. In the second article, describing the same two nests (Varricchio et al., 1999) these suggestions turn to facts: The nest protected the eggs by creating a suitable micro-environment during the lengthy egg-laying and incubation periods. . . Some reproductive features typically associated with living birds rst evolved within non-avian coelurosaurian theropods like Troodon. These conclusions are cited without any caveats in review articles by Padian and Chiappe (1998) and Prum (2002); so by repetition, they are becoming an orthodoxy. Deeming (2002), after examination of published data on positioning of eggs in the Oviraptors nests and on the egg size, shape, and shell structure concludes that the Oviraptors eggs were almost certainly completely covered by substrate, most likely sand, and the animal was laying on top of nest mound, rather than sitting directly on top of the eggs. Contact incubation was not possible. The possibility of Troodon incubating eggs has not been critically scrutinized so far. The conjectures of Varricchio et al. (1997) on ovulation patterns and lengthy egg-laying periods are based exclusively on the egg arrangement in one of the nests. However, the positioning of eggs need not be in any way dependent on the temporal pattern of laying-even mass-laying organisms lay consecutively, only one egg at a time. Thus, laying females have behavioral control of placement of their consecutive eggs. For example, although all birds lay eggs singly at long intervals, they either put all eggs into a single nest or deposit eggs in several nests (brood parasites). Summing up, the paleontological data demonstrate the existence of early forms of parental care (nest guarding) in some theropod dinosaurs, but contrary to the claims, they do not provide solid evidence for the existence of contact incubation or presence of lengthy egg-laying periods in any theropod species. Therefore, for the time being, the two latter features should be treated, as before, as unique avian traits. Parental care in crocodiles, dinosaurs, and birds: homologous or analogous? Varricchio et. al. (1999) and Prum (2002) propose that parental care is primitive in Archosuaria. Tullberg et al. (2002) and Burley and Johnson (2002) share this view and indicate females as the caring sex. They propose that the common ancestor of crocodilians dinosaurs and birds was an animal in which females provided parental care. Thus, the presence of parental care in the extant crocodilians and birds is a homologous trait, derived from the common ancestor. This is the most parsimonious explanation. However, the most parsimonious answer is not automatically true (for review, see Harvey and Pagel, 1991). Parsimony is only a useful analytical tool, and not an intransgressible law of nature; it cannot be used to dismiss other possibilities without even considering them. What other arguments, besides parsimony, speak in favor of homologous origin and/or against independent origin of parental care in birds and crocodiles? Generally, any homology assumption would be well supported if (1) the trait considered was unique and/or complicated (its origin would be very improbable or difcult), (2) the compared groups were close relatives, and (3) differences were of only quantitative character. None of these conditions seem to hold in the crocodile-bird case.

The initial steps of parental care evolution (egg/young guarding) have been independently reached by many organisms in many major invertebrate and vertebrate groups (for review, see Clutton-Brock, 1991; Reynolds et al., 2002), so such behavior evolves easily and the presence of egg guarding in crocodiles is not anything unique, anything that could not independently evolve in different lineages of Archosauria. Though crocodiles are closest living relatives of birds, they are nevertheless only distantly related, the last common ancestor of birds and crocodiles lived more than 200 (possibly as long as 260) million years ago (Broom, 1913; Walker, 1972). We do not know anything about the presence of parental care and its form in this ancestor or in its descendants leading to birds and crocodiles, respectively. In proposing homology, we have to assume that in all of these forms females guarded eggs, that no cases of care loss and regaining could have occurred. It is unclear how this assumption could hold true, when only within Chardriformes, a single order of birds, several independent instances of maternal care gain and loss took place (Sze kely and Reynolds, 1995). Thorough knowledge of phylogenetic relationships among different groups of fossil reptiles/early birds and their breeding habits would be critical in resolving the homology issue and in reconstructing consecutive evolutionary transitions of parental care patterns. Recent surge of discoveries of new fossils of early birds (for review, see Padian and Chiappe, 1998; Prum, 2002) brings some hope for the future, but currently we are rather far from this goal; relationships among different lineages are still hotly debated (for review, see Prum, 2002). In a situation in which most taxa are missing from the reconstructed phylogenies, the usage of formal cladistic analysis cannot be of much help in resolving the problem (Burley and Johnson, 2002; Grant, 2001; Harvey and Pagel, 1991; Schluter et al., 1997). The results of such analysis of patterns of parental care in birds and other terrestrial vertebrates by Tullberg et al. (2002) clearly demonstrate the limitations of the cladistic techniques in such circumstances. Their cladograms suggest several quite unrealistic evolutionary scenarios; that is, maternal care would be primitive not only in Archosuaria, but in all reptiles (parental care in mammals and crocodiles would be homologous), and maternal care would be lost in Chelonia and Squamata. Taken together, the above arguments indicate that in the crocodile-bird case the homology hypothesis seems very weakly substantiated, so the possibility of independent origins of parental care has to be seriously considered in any attempts to reconstruct the evolution of parental care in different Archosaurian lineages (Ligon, 1999; Wesoowski, 1994). Could paternal care in birds evolve rst? Burley and Johnson (2002) think not. They maintain that the arguments for the male care rst hypothesis have not been presented in sufcient detail, and they raise several issues (nest building, anisogamy, paternity certainty, and incubation) purported to prevent the evolution of paternal care but apparently not adequately covered. However, to large extent, Burley and Johnson (2002) criticize arguments never put forward in the original models. They impute that a male care rst scenario would require that birds evolved from an ancestor in which females showed no preparation of nest site. . . after evolving surface nesting, whereas Wesoowski (1994) proposed that initially there was no post-ovipositional egg care and that the ancestors of birds probably buried eggs in reptilian fashion. Similarly, nowhere in Wesoowski (1994) is there a slightest hint, suggesting that the continuous incubation of eggs could have occurred in the rst stages of

Downloaded from http://beheco.oxfordjournals.org/ by guest on April 23, 2013

522

Behavioral Ecology Vol. 15 No. 3

evolution, yet Burley and Johnson (2002) claim that paternal care could not evolve because continuous incubation would compromise a males ability to defend his territory an locate additional mates. Several paragraphs in Wesoowski (1994) are devoted to discussion of the certainty of paternity problem. In line with arguments put forward by numerous investigators (for review, see Clutton-Brock, 1991), conditions in which parental males could combine female attraction, paternity assurance, and egg guarding were specied. Briey, males controlling access to the laying grounds could trade copulations for egg-laying; females would not be permitted to lay eggs within a territory without having rst copulating and staying for some time with the territory owner. Moreover, recent molecular studies on Jacana jacana (Emlen et al., 1998) and Struthio camelus (Kimwele and Graves, 2003), showing high frequency of mixed brood paternity, demonstrate that the extensive paternal care can co-occur with low paternity certainty. Burley and Johnson (2002) do not question these arguments, yet they raise the lack of paternity certainty to dismiss the possibility of sole male care evolution. The last of arguments against the paternal care rst put forward by them is anisogamy. It is true that there is a built-in asymmetry in the no care situation, because females have to choose nest sites, prepare laying sites, and lay eggs before leaving the place. The appearance of paternal care in such conditions constitutes really a challenge, as birds are the most anisogamous of animals. However, anisogamy itself does not constitute an insurmountable hurdle. Sole paternal care has evolved many times in different organisms (invertebrates, shes, or amphibians; for review, seen Clutton-Brock, 1991; Reynolds et al., 2002). The problem of why avian males engage so frequently in parental care, despite extreme anisogamy, is fully recognized by Wesoowski (1994); large sections of this article are devoted to addressing this puzzle. Problems with the paternal care rst scenarios seem to be caused to a large extent by misunderstanding of their arguments by Burley and Johnson (2002) and not by serious biological aws inherent in these scenarios. Refutation of the no to sole paternal care avenue of the parental care origins in birds would demand providing arguments stronger than those currently available. Therefore, for the time being, this scenario should remain a working hypothesis, worth further testing. Requirements of a comprehensive theory of the parental care origin in birds As follows from the previous discussion, the issue of parental care origins in birds is still controversial and will (hopefully) stimulate further theoretical and empirical work in the years to come. However, it seems that suggesting some guidelines and some minimum methodical requirements that the future proposals should abide would be helpful in making these efforts more efcient. First of all, the models should simultaneously account for all the existing patterns: origins of surface nesting, sequential ovulation, incubation, enormous increase in egg size, change of copulatory mode combined with loss of phallus (Frey, 1995; Wesoowski, 1999), and participation of each sex in parental duties. They should relate these traits to the appearance of features connected with powered ight (high metabolic rate, endothermy, determinate growth, very fast growth rates, stiffening of trunk, and shortening of abdomen). They should also propose a relative timing for all of these events, as well as relationships among them-which factors were causal, which permissive, and which necessary but insufcient themselves (e.g., whether sequential ovulation evolved before or after onset of incubation, what selective agents lay behind the

development of the former or the latter). They also have to account for the known taxonomic distribution of different care modes; that is, they should propose why uniparental female care in extant birds occurs in several separate lineages situated near the tips of phylogenetic branches, whereas groups with uniparental male care or with sole male incubation are situated close to the base of the tree (Sze kely and Reynolds, 1995; Vehrencamp, 2000). They have to explain, as well, the existence of superprecociality in at least some Upper Cretaceous Enatiornithes, (young of Gobipteryx were able to y shortly after hatching; Elz _ anowski, 1985). All these explanations must be internally coherent. A question of monophyletic versus parallel origin of parental care in birds should be addressed as well. All cost/benet analyses of parental options must not use good for the opposite sex arguments (it would be good for females if males). This is important because tness can be compared only within a sex. Whether one sex evolves care is not dependent upon advantages or disadvantages to the other sex but on tness differences of same-sex individuals showing versus nonshowing a given type of behavior (Fisher, 1958; Maynard Smith, 1977). Finally, a more critical evaluation of evidence, both already known and forthcoming in future work (especially of fossil data) should be made before drawing any inferences. Specifically, using the physical association of a fossil animal with eggs, without examining all the available evidence, as a sole argument for the existence of incubation, should be avoided, as it can lead to the wrong conclusions (Deeming, 2002). I do hope that if future models are prepared according to these specications, it would bring us closer to the nal goalreconstruction of the actual history of the of parental care origin in birds.
I am grateful to all the people who have recently published articles on the origins of parental care in birds. Although sometimes I disagree with their arguments, their work has inspired me to rethink my ideas on this subject and stimulated me to write these comments. I also highly appreciate comments of Sandra Vehrencamp and anonymous refrees on an earlier draft of this manuscript. Address correspondence to T. Wesoowski. E-mail: tomwes@biol.uni. wroc.pl. Received 14 February 2003; revised 5 July 2003; accepted 17 August 2003.

Downloaded from http://beheco.oxfordjournals.org/ by guest on April 23, 2013

REFERENCES
Broom R, 1913. On the South African pseudosuchian Euparkeria and allied genera. Proc Zool Soc Lond 1913:619633. Burley NT, Johnson K, 2002. The evolution of avian parental care. Phil Trans R Soc Lond B 357:241250. Clutton-Brock TH, 1991. The evolution of parental care. Princeton, New Jersey: Princeton University Press. Deeming DC, 2002. Importance and evolution of incubation in avian reproduction. In: Avian incubation (Deeming DC, ed). Oxford: Oxford University Press; 17. Elz _ anowski A, 1985. The evolution of parental care in birds with reference to fossil embryos. In: Acta XVIII Congressus Internationalis Ornithologici, Moscow, 1982, vol. 1 (Ilyichev VD, Gavrilov VM, eds). Moscow: Nauka; 178183. Emlen ST, Wrege PH, Webster MS, 1998. Cuckoldry as a cost of polyandry in the sex-role reversed wattled jacana, Jacana jacana. Proc R Soc Lond B 265:23592364. Fisher RA, 1958. The genetical theory of natural selection. New York: Dover. Frey R, 1995. Copulatory organ, mating posture and locomotion: their interrelationship in non-mammalian vertebrates. J Zool Syst Evol Res 33:1731.

Wesoowski

Origin of parental care in birds

523

Grant PR, 2001. Reconstructing the evolution of birds on islands: 100 years of research. Oikos 92:385403. Handford P, Mares MA, 1985. The mating systems of ratites and tinamous: an evolutionary perspective. Biol J Linn Soc 25:77104. Harvey PH, Pagel MD, 1991. The comparative method in evolutionary biology. Oxford: Oxford University Press. Kavanau JL, 1987. Lovebirds, cockatiels, budgerigars: behavior and evolution. Los Angeles: Science Software Systems. Kendeigh SC, 1952. Parental care and its evolution in birds. Illinois Biol Mon 22:1358. Kimwele CN, Graves JA, 2003. A molecular genetic analysis of the communal nesting of the ostrich (Struthio camelus). Mol Ecol 12: 229236. Ligon JD, 1999. The evolution of avian breeding systems. Oxford: Oxford University Press. Maynard Smith J, 1977. Parental investment: a prospective analysis. Anim Behav 25:19. Norell MA, Clark JM, Chiappe LM, Dashzeveg D, 1995. A nesting dinosaur. Nature 378:774776. wiat Nauki 4: Padian K, Chiappe LM, 1998. Ska d sie wzie y ptaki. S 2635. Prum RO, 2002. Why ornithologists should care about the theropod origin of birds. Auk 119:117. Reynolds JD, Goodwin NB, Freckleton RP, 2002. Evolutionary transitions in parental care and live bearing in vertebrates. Phil Trans R Soc Lond B 357:269281.

Schluter D, Price T, Mooers AO, Ludwig D, 1997. Likelihood of ancestor states in adaptive radiation. Evolution 51:16991711. Sze kely T, Reynolds JD, 1995. Evolutionary transitions in parental care in shorebirds. Proc R Soc Lond B 262:5764. Tullberg BS, Ah-King M, Temrin H, 2002. Phylogenetic reconstruction of parental-care systems in the ancestors of birds. Phil Trans R Soc Lond B 357:251257. van Rhijn J, 1984. Phylogenetical constraints in the evolution of parental care strategies in birds. Neth J Zool 34:103122. van Rhijn JG, 1990. Unidirectionality in the phylogeny of social organization, with special reference to birds. Behaviour 115:53174. Varricchio DJ, Jackson F, Borkowski JJ, Horner JR, 1997. Nest and egg clutches of the dinosaur Troodon formosus and the evolution of avian reproductive traits. Nature 385:247250. Varricchio DJ, Jackson F, Treuman CN, 1999. A nesting trace with eggs for the Cretaceous theropod dinosaur Troodon formosus. J Vert Paleont 19:91100. Vehrencamp SL, 2000. Evolutionary routes to joint-female nesting in birds. Behav Ecol 11:334344. Walker A.D, 1972. New light on the origin of birds and crocodiles. Nature 237:257263. Wesoowski T, 1994. On the origin of parental care and the early evolution of male and female parental roles in birds. Am Nat 143: 3958. Wesoowski T, 1999. Reduction of phallus in birds: an avian way to safe sex? J Avian Biol 30:483485.

Downloaded from http://beheco.oxfordjournals.org/ by guest on April 23, 2013