Fabien Aubret

Evolutionary biology: Adaptive developmental plasticity in snakes

The morphology of organisms is generally well matched to their environment, presumably because expression of their genes is tailored either at the population or the individual level to suit local conditions: for example, snake populations that persistently encounter large prey may accumulate gene mutations that specify a large head size, or head growth may be increased in individual snakes to meet local demands (adaptive developmental plasticity). Here we test the relative contributions of genetics and environment to the jaw sizes of two tiger snake populations: one that consumes small prey on the mainland, and an island population that relies on larger prey and has a larger jaw size. Although the idea of adaptive plasticity in response to environmental pressures is controversial, we find that both factors influence the difference in jaw size between the two populations, and the influence of developmental plasticity is greater in the island population.

Fat Is Sexy for Females but Not Males: The Influence of Body Reserves on Reproduction in Snakes (Vipera aspis)

Reproduction is energetically expensive for both sexes, but the magnitude of expenditure and its relationship to reproductive success differ fundamentally between males and females. Males allocate relatively little to gamete production and, thus, can reproduce successfully with only minor energy investment. In contrast, females of many species experience high fecundity-independent costs of reproduction (such as migration to nesting sites), so they need to amass substantial energy reserves before initiating reproductive activity. Thus, we expect that the relationship between energy reserves and the intensity of reproductive behavior involves a threshold effect in females, but a gradual (or no) effect in males. We tested this prediction using captive vipers (Vipera aspis), dividing both males and females into groups of high versus low body condition. Snakes from each group were placed together and observed for reproductive behavior; sex-steroid levels were also measured. As predicted, females in below-average body condition had very low estradiol levels and did not show sexual receptivity, whereas males of all body condition indices had significant testosterone levels and displayed active courtship. Testosterone levels and courtship intensity increased gradually (i.e., no step function) with body condition in males, but high estradiol levels and sexual receptivity were seen only in females with body reserves above a critical threshold.

Thermal plasticity in young snakes: how will climate change affect the thermoregulatory tactics of ectotherms?

SUMMARY Climate change will result in some areas becoming warmer and others cooler, and will amplify the magnitude of year-to-year thermal variation in many areas. How will such changes affect animals that rely on ambient thermal heterogeneity to behaviourally regulate their body temperatures? To explore this question, we raised 43 captive-born tiger snakes Notechis scutatus in enclosures that provided cold (19–22°C), intermediate (19–26°C) or hot (19–37°C) thermal gradients. The snakes adjusted their diel timing of thermoregulatory behaviour so effectively that when tested 14 months later, body temperatures (mean and maximum), locomotor speeds and anti-predator behaviours did not differ among treatment groups. Thus, the young snakes modified their behaviour to compensate for restricted thermal opportunities. Then, we suddenly shifted ambient conditions to mimic year-to-year variation. In contrast to the earlier plasticity, snakes failed to adjust to this change, e.g. snakes raised at cooler treatments but then shifted to hot conditions showed a higher mean body temperature for at least two months after the onset of the new thermal regime. Hence, thermal conditions experienced early in life influenced subsequent thermoregulatory tactics; the mean selected temperature of a snake depended more upon its prior raising conditions than upon its current thermoregulatory opportunities. Behavioural plasticity thus allows snakes to adjust to suboptimal thermal conditions but this plasticity is limited. The major thermoregulatory challenge from global climate change may not be the shift in mean values (to which our young snakes adjusted) but the increased year-to-year variation (with which our snakes proved less able to deal).

Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal

Predation is a strong selective pressure generating morphological, physiological and behavioural responses in organisms. As predation risk is often higher during juvenile stages, antipredator defences expressed early in life are paramount to survival. Maternal effects are an efficient pathway to produce such defences. We investigated whether maternal exposure to predator cues during gestation affected juvenile morphology, behaviour and dispersal in common lizards (Zootoca vivipara). We exposed 21 gravid females to saurophagous snake cues for one month while 21 females remained unexposed (i.e. control). We measured body size, preferred temperature and activity level for each neonate, and released them into semi-natural enclosures connected to corridors in order to measure dispersal. Offspring from exposed mothers grew longer tails, selected lower temperatures and dispersed thrice more than offspring from unexposed mothers. Because both tail autotomy and altered thermoregulatory behaviour are common antipredator tactics in lizards, these results suggest that mothers adjusted offspring phenotype to risky natal environments (tail length) or increased risk avoidance (dispersal). Although maternal effects can be passive consequences of maternal stress, our results strongly militate for them to be an adaptive antipredator response that may increase offspring survival prospects.

Fitness costs may explain the post-colonisation erosion of phenotypic plasticity

SUMMARY Many organisms can adjust their phenotypes to match local environmental conditions via shifts in developmental trajectories, rather than relying on changes in gene frequencies wrought by natural selection. Adaptive developmental plasticity confers obvious benefits in terms of rapid response and higher mean fitness, so why is it not more common? Plausibly, adaptive plasticity also confers a cost; reshaping the phenotype takes time and energy, so that canalised control of trait values enhances fitness if the optimal phenotype remains the same from one generation to the next. Although this idea is central to interpreting the fitness consequences of adaptive plasticity, empirical data on costs of plasticity are scarce. In Australian tiger snakes, larger relative head size enhances maximal ingestible prey size on islands containing large prey. The trait arises via adaptive plasticity in snake populations on newly colonised islands but becomes genetically canalised on islands where snakes have been present for much longer periods. We experimentally manipulated relative head size in captive neonatal snakes to quantify the costs of adaptive plasticity. Although small-headed snakes were able to increase their head sizes when offered large prey, the delay in doing so, and their inability to consume large prey at the outset, significantly reduced their growth rates relative to conspecifics with larger heads at the beginning of the experiment. This study describes a proximate cause to the post-colonisation erosion of developmental plasticity recorded in tiger snake populations.

Aquatic locomotion and behaviour in two disjunct populations of Western Australian tiger snakes, Notechis ater occidentalis

Adaptive phenotypic plasticity can be viewed as an evolutionary strategy that enables organisms to match their phenotypes to local conditions. I studied two neighbouring populations of amphibious fresh-water tiger snakes, Notechis ater occidentalis, from Western Australia. One mainland population occurs around a lake, feeds primarily on frogs, and is under strong predation pressure, whereas the second population inhabits a small offshore island with no standing water and no known predators, and feeds primarily on chicks. The availability of water and its use as a habitat differ considerably between the two populations. I compared experimentally the locomotor capacities and behaviour of individuals from both populations in water, treating neonates and adults separately. Sex did not significantly influence any trait in both populations, in either adults or neonates. At birth, the two populations exhibited very little difference in swimming speed, stamina, apnoea capacities or behaviour. However, adult mainland snakes had greater apnoea capacities and faster burst swimming speed than island snakes. Mainland adult snakes also spontaneously swam underwater for longer, and a higher proportion filled their lungs while surface swimming compared with island specimens. This study suggests strong behavioural flexibility in tiger snakes depending on habitats. ZO ocbeha i a F t

Early Experience Influences both Habitat Choice and Locomotor Performance in Tiger Snakes

Through adaptive developmental plasticity, individuals may function most effectively in the type of environment in which they have spent most of their time. Such habitat‐specific modifications may favor active selection of that habitat type later in life, further reinforcing developmentally plastic phenotypic modifications. The interaction between these processes may have profound evolutionary implications. In nature, Australian tiger snakes (Notechis scutatus) use a complex mosaic of terrestrial, arboreal, and aquatic habitats. We raised juvenile tiger snakes for the first 11 months of life in enclosures mimicking one of these habitats and then tested their habitat selection when offered a choice of habitat types. Snakes consistently selected the habitat types in which they had been reared, and they were more effective at locomotion in those habitats than in the others. This attachment to a familiar habitat and phenotypically flexible adjustments in order to function effectively in that habitat constitute a positive feedback loop. That is, animals benefit by choosing a familiar habitat because they can fine‐tune behaviors in ways that enable them to function better in that habitat, and, by consistently selecting that kind of habitat, they not only reinforce those phenotypically plastic adjustments but also are placed under continuing selection to cope with the challenges (of foraging, predator evasion, etc.) imposed by that habitat type. The end result may be to create ecomorphs, whereby different individuals within a population become specialized for different types of habitats even in the absence of genetic differentiation.

Body-size evolution on islands: are adult size variations in tiger snakes a nonadaptive consequence of selection on birth size?

Mean adult size has been used as the traditional measure of body size to explain trends of insular gigantism and dwarfism in a wide array of taxa. However, patterns of variation in body size at birth have received surprisingly little attention, leaving open the possibility that adult body-size differences are nonadaptive consequences of selection acting on neonate body size. Here I used an empirical and correlative approach to test this hypothesis in a mosaic of 12 island and mainland snake populations in Australia. Data collected on 597 adult and 1,084 neonate tiger snakes showed that (1) both adult and neonate mean body sizes varied strongly across populations; (2) prey diversity and size convincingly explained birth-size variations: birth size—notably, gape size—correlated with prey size; (3) neonate snout-vent length was significantly correlated with neonate gape size; and (4) neonate snout-vent length was significantly correlated with adult snout-vent length. Postnatal growth rates recorded under common-garden conditions differed across populations and were correlated with mean prey size. These data collectively suggest that (1) prey size is the main driver for the evolution of body size at birth in gape-limited predators, (2) adult size variations may reflect selective forces acting on earlier life stages, and (3) adult size variations may also reflect resource availability during ontogeny (notably, prey diversity).

Heartbeat, embryo communication and hatching synchrony in snake eggs

Communication is central to life at all levels of complexity, from cells to organs, through to organisms and communities. Turtle eggs were recently shown to communicate with each other in order to synchronise their development and generate beneficial hatching synchrony. Yet the mechanism underlying embryo to embryo communication remains unknown. Here we show that within a clutch, developing snake embryos use heart beats emanating from neighbouring eggs as a clue for their metabolic level, in order to synchronise development and ultimately hatching. Eggs of the water snake Natrix maura increased heart rates and hatched earlier than control eggs in response to being incubated in physical contact with more advanced eggs. The former produced shorter and slower swimming young than their control siblings. Our results suggest potential fitness consequences of embryo to embryo communication and describe a novel driver for the evolution of egg-clustering behaviour in animals.

Phylogeography and conservation genetics of the common wall lizard, Podarcis muralis, on islands at its northern range.

Populations at range limits are often characterized by lower genetic diversity, increased genetic isolation and differentiation relative to populations at the core of geographical ranges. Furthermore, it is increasingly recognized that populations situated at range limits might be the result of human introductions rather than natural dispersal. It is therefore important to document the origin and genetic diversity of marginal populations to establish conservation priorities. In this study, we investigate the phylogeography and genetic structure of peripheral populations of the common European wall lizard, Podarcis muralis, on Jersey (Channel Islands, UK) and in the Chausey archipelago. We sequenced a fragment of the mitochondrial cytochrome b gene in 200 individuals of P. muralis to infer the phylogeography of the island populations using Bayesian approaches. We also genotyped 484 individuals from 21 populations at 10 polymorphic microsatellite loci to evaluate the genetic structure and diversity of island and mainland (Western France) populations. We detected four unique haplotypes in the island populations that formed a sub-clade within the Western France clade. There was a significant reduction in genetic diversity (HO, HE and AR) of the island populations in relation to the mainland. The small fragmented island populations at the northern range margin of the common wall lizard distribution are most likely native, with genetic differentiation reflecting isolation following sea level increase approximately 7000 BP. Genetic diversity is lower on islands than in marginal populations on the mainland, potentially as a result of early founder effects or long-term isolation. The combination of restriction to specific localities and an inability to expand their range into adjacent suitable locations might make the island populations more vulnerable to extinction.