Predation Drives Interpopulation Differences in Parental Care Expression
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Journal of Animal Ecology 2013, 82, 429–437 doi: 10.1111/1365-2656.12015 Predation drives interpopulation differences in parental care expression Wen-San Huang1*, Si-Min Lin2, Sylvain Dubey3 and David A. Pike4 1Department of Zoology, National Museum of Natural Science, Taichung 404, Taiwan; 2Department of Life Science, National Taiwan Normal University, Taipei 116, Taiwan; 3Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland; and 4School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4812, Australia Summary 1. Expressing parental care after oviposition or parturition is usually an obligate (evolved) trait within a species, despite evolutionary theory predicting that widespread species should vary in whether or not they express parental care according to local selection pressures. The lizard Eutropis longicaudata expresses maternal care only in a single population throughout its large geographical range, but why this pattern occurs is unknown. 2. We used reciprocal translocation and predator exclusion experiments to test whether this intraspecific variation is a fixed trait within populations and whether predator abundance explains this perplexing pattern. 3. Wild-caught female lizards that were reciprocally translocated consistently guarded or abandoned eggs in line with their population of origin. By contrast, most lizards raised in a common garden environment and subsequently released as adults adopted the maternal care strategy of the recipient population, even when the parents originated from a population lack- ing maternal care. 4. Egg predation represents a significant fitness cost in the populations where females display egg-guarding behaviour, but guarding eggs outweighs this potential cost by increasing hatch- ing success. 5. These results imply that predators can be a driving force in the expression of parental care in instances where it is normally absent and that local selection pressure is sufficient to cause behavioural divergence in whether or not parental care is expressed. Key-words: behavioural plasticity, islands, maternal care, parental care evolution, reciprocal translocation (Tallamy 1984; Clutton-Brock 1991; Wesoowski 1994). Introduction The general life-history circumstances favouring parental Animals have evolved a wide range of parental care strat- care thus include low egg or juvenile survival without egies to increase offspring survival, ranging from nest-site- care, relatively long egg incubation periods and relatively guarding to much more complex provisioning behaviours short juvenile stages (Clutton-Brock 1991; Klug & Bonsall (Clutton-Brock 1991; Wesoowski 1994; Klug & Bonsall 2009), while the general ecological circumstances favour- 2009). These strategies have evolved independently numer- ing parental care include food availability and predation ous times in disparate animal lineages, providing strong risk (Lack 1968; Tallamy & Wood 1986). Overall, species evidence of their success as an evolutionary strategy for are more likely to evolve parental care when the risk of increasing fitness (Tallamy 1984; Shine 1988; Clutton- predation on eggs or offspring is high (Lack 1968; Brock 1991; Gross 2005). Evolutionary theory predicts Tallamy & Wood 1986). that parental care should evolve from a nonparental Parental care is any action of the parent after oviposi- caring ancestral state when the fitness benefits accrued by tion or parturition that increases the chances of survival protecting offspring outweigh the costs of providing care of the offspring (Shine 1988; Greene et al. 2002). For example, within single populations of cichlid fish (Sarotherodon galilaeus Linnaeus 1758) and birds (Remiz *Correspondence author. E-mail: [email protected] pendulinus Linnaeus 1758), parental care can be provided © 2012 The Authors. Journal of Animal Ecology © 2012 British Ecological Society 430 W.-S. Huang et al. by both parents or by either one of the sexes alone and increases the proportion of eggs that hatch, offspring (Persson & O¨ hrstro¨ m 1989; Balshine-Earn & Earn 1998). growth rates, and survival (Huang & Pike 2011b). Furthermore, the type and intensity of parental care However, this behaviour is costly because eggs laid inside behaviours expressed can vary with offspring development the retaining wall are exposed to predators throughout (reviewed by Magnhagen 1992) or local environmental incubation, as compared with eggs buried beneath cover conditions (Dunn & Robertson 1992; Wheelwright, objects in natural habitat (Huang & Pike 2011b). Despite Schultz & Hodum 1992; Sze´ kely & Cuthill 1999). Thus, the increased risk of predators locating eggs laid inside of many widespread species show differences within and these retaining walls, female long-tailed skinks from 12 among populations in the duration, type or intensity of other populations (11 from the island of Taiwan and one parental care (e.g. Dunn & Robertson 1992; Wheelwright, from Green Island, all nesting in similar retaining walls) Schultz & Hodum 1992; Sze´ kely & Cuthill 1999; Webb abandon their eggs immediately after oviposition (W.-S. et al. 1999), but almost all species expressing parental care Huang, unpublished). Thus, the expression of parental are known to do so throughout their entire geographical care is not a fixed trait shared among populations (i.e. range. By contrast, examples of parental care expression obligate; as it appears to be in all other species) because in some populations but not others are extremely rare; only the females nesting inside the retaining wall on known examples include a frog (Martins, Pombal & Had- Orchid Island express parental care. As in many other dad 1999) and, if we consider maternal care to occur taxa, not all females remain with the eggs for the entire throughout the entire duration of pregnancy, lizard incubation period (but they still initially express, and thus species with both oviparous and viviparous populations provide, maternal care; Huang & Wang 2009). The dura- (e.g. Heulin et al. 1999). Other rare cases include nest tion of maternal nest-guarding depends on the risk of egg abandonment in species which provision their offspring, predation: when egg-eating snakes are rare, females leave which almost always results in offspring death (e.g. Burley the nest early in incubation, but when snakes are abun- & Johnson 2002; Reynolds, Goodwin & Freckleton 2002). dant, females continue defending the nest until the eggs Parental care is thus almost always expressed throughout hatch (Huang & Wang 2009). This suggests that local the entire distribution of most species. This evolutionary predation pressure plays an important role in the evolu- pattern limits our capacity to unravel the selective tion of maternal care. We can test this hypothesis using pressures leading to the evolution of parental care (Clut- reciprocal translocation experiments to test directly ton-Brock 1991; Wesoowski 1994; Gross 2005). It also whether exposing female lizards to local ecological condi- seems to contradict the notion that because widespread tions they normally would not experience will alter the species are under different selection pressures throughout expression of parental care behaviour from that of the their geographical range, they should express parental source population. care in line with predation risk, so as to maximize An additional hypothesis for the facultative parental offspring survival. Why, then, do most widespread species care expression in long-tailed skinks is that geographical show obligate parental care expression, rather than facul- isolation has resulted in substantial genetic divergence, tative care, where adults adjust whether they provide or where the diverged population now provides maternal do not provide parental care according to the threat of care. This would mean that other populations do not have predation of the offspring? This situation would only per- the capacity to express maternal care, and thus would not sist in species where the offspring can physically survive do so, even under the ecological circumstances in which without relying on either of the parents (e.g. many rep- other (genetically diverged) individuals do provide care. tiles, amphibians and invertebrates; Shine 1988). We would then expect the long-tailed skink population on Long-tailed skinks (Eutropis longicaudata Hallowell Orchid Island to represent a highly divergent lineage 1857) are widely distributed throughout South-East Asia (or possibly even a separate, but morphologically similar, and only express parental care in a single population on species). The straight separating the island of Taiwan Orchid Island, located off the south-eastern coast of from Orchid Island is sufficiently deep (>1 km) that Taiwan (Huang 2004). In this population, mothers nest- Orchid Island has never been connected with other ing within concrete retaining walls remain at the nest dur- islands, even during low sea levels of the last glacial maxi- ing incubation and actively deter egg-eating snakes mum (LGM). Consequently, we might expect an absence (Oligodon formosanus Gu¨ nther 1872) from entering the of shared haplotypes between Orchid Island and the other nest and consuming the eggs (Huang 2006a; Supplemen- populations and perhaps the presence of distinct genetic tary Information S1). Antisnake behaviour is only lineages there. Parental care can have an underlying expressed while gravid, immediately prior to oviposition genetic component; for example, mice lacking the fosB