Adaptive developmental plasticity in snakes

Aubret, Fabien; Shine, Richard; Bonnet, Xavier

doi:10.1038/431261a

Cited by 117 publications

(107 citation statements)

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“…ongoing impact and an adaptive response to that impact or, alternatively, to developmental changes in head growth associated with dietary change subsequent to the arrival of toads. Although early studies reported that relative HS in snakes were not developmentally plastic with respect to temperature (32,33), recent studies provide evidence that relative HS in snakes can shift as a consequence of differences in mean prey size (34)(35)(36).…”

Section: Discussionmentioning

confidence: 99%

Adapting to an invasive species: Toxic cane toads induce morphological change in Australian snakes

Phillips

Shine

2004

Proc. Natl. Acad. Sci. U.S.A.

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247

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The arrival of invasive species can devastate natural ecosystems, but the long-term effects of invasion are less clear. If native organisms can adapt to the presence of the invader, the severity of impact will decline with time. In Australia, invasive cane toads (Bufo marinus) are highly toxic to most snakes that attempt to eat them. Because snakes are gape-limited predators with strong negative allometry for head size, maximum relative prey mass (and thus, the probability of eating a toad large enough to be fatal) decreases with an increase in snake body size. Thus, the arrival of toads should exert selection on snake morphology, favoring an increase in mean body size and a decrease in relative head size. We tested these predictions with data from specimens of four species of Australian snakes, collected over >80 years. Geographic information system layers provided data on the duration of toad exposure for each snake population, as well as environmental variables (latitude, precipitation, and temperature). As predicted, two toad-vulnerable species (Pseudechis porphyriacus and Dendrelaphis punctulatus) showed a steady reduction in gape size and a steady increase in body length with time since exposure to toads. In contrast, two species at low risk from toads (Hemiaspis signata and Tropidonophis mairii) showed no consistent change in these morphological traits as a function of the duration of toad exposure. These results provide strong evidence of adaptive changes in native predators as a result of the invasion of toxic prey.adaptation ͉ conservation ͉ contemporary evolution ͉ coevolution H uman-induced environmental change is the greatest threat to global biodiversity. Such processes include global climate change, invasive species, habitat removal, overharvesting, and altered biogeochemical cycles (1-3). These changes have caused many extinctions (local and global) and will lead to many more, but whenever the impact is nonrandom (i.e., selective), there is the potential for adaptive evolution. Under the right circumstances, adaptive evolution can happen very rapidly in wild populations. Such ''contemporary evolution'' (see ref. 4) occurs as a consequence of selection during natural events (e.g., refs. 5-7). Importantly, however, it has also been documented from ''unnatural'' (human-mediated) events. The classic example of industrial melanism in peppered moths is the most celebrated case (8, 9); however, there is also clear evidence of adaptive evolution in populations as a consequence of overfishing (10), global warming (11), and heavy-metal pollution (12).These studies highlight the importance of examining the potential for adaptive change in impacted populations. Doing so can clarify both the nature of the impact and the response of the affected population. Clearly, a population exhibiting an adaptive response is more likely to persist in the face of an environmental change than one that fails to adapt. Invasive species are of particular interest in this respect because they are believed to constitute a major ...

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Section: Discussionmentioning

confidence: 99%

Adapting to an invasive species: Toxic cane toads induce morphological change in Australian snakes

Phillips

Shine

2004

Proc. Natl. Acad. Sci. U.S.A.

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247

190

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“…In the early stages of colonisation, adaptive plasticity in head growth rates may have provided an advantage to young snakes, where larger prey size stimulated a shift in relative head size as well as body size (that is, as a consequence of enhanced feeding success- Aubret et al, 2004a;Aubret and Shine, 2009). As prey size drove the evolution of snake body size at birth (Aubret, 2012), I expected a clear match between prey size available and snake body size in long isolated populations as well as mainland snake populations.…”

Section: Discussionmentioning

confidence: 99%

“…Mainland Tiger snakes typically produce litters composed of numerous small neonates that feed on a wide range of small prey items (Aubret, 2012). Insularity created a potentially huge mismatch between prey size and neonate swallowing ability (that is, due to drastically different prey assemblages), generating intense selective pressure for an increase in body and head size of neonate snakes (Forsman, 1991;King, 2002;Aubret et al, 2004a; Figure 3 Body mass rates of evolution and levels of adaptive plasticity. Rates of evolution in body mass in grams per generation were significantly correlated with the level of plasticity for head growth in response to prey size calculated for five island populations (linear regression; R 2 ¼ 0.88; F 1, 3 ¼ 21.14; Po0.019).…”

Section: Discussionmentioning

confidence: 99%

“…Although a number of hypotheses have been suggested to explain these rapid body size shifts (that is, competition, predation and sexual selection), natural selection acting to optimise snake body size to available prey size is strongly supported by the correlation between snake size and available prey size (Schwaner, 1985;Shine, 1987;Sarre, 1988, 1990;Aubret, 2012). Recent work suggested that larger prey present on islands have generated selective regimes driving increased body and head size at birth in these gape-limited predators, as well as increased levels of adaptive plasticity in head growth in response to prey size (Ehrlich, 1989;Holway and Suarez, 1999;West-Eberhard, 2003;Aubret et al, 2004a;Aubret and Shine, 2007;Aubret, 2012). Although young snakes from recently isolated populations (that is, o6000 years) were experimentally shown to be able to accelerate head growth, and hence swallowing performance, in response to large prey (Aubret and Shine, 2009), snakes from older islands no longer exhibited plasticity in response to prey size but were in turn born larger: the trait had been genetically assimilated (Waddington, 1942(Waddington, , 1953Pigliucci et al, 2006).…”

Section: Introductionmentioning

confidence: 94%

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Island colonisation and the evolutionary rates of body size in insular neonate snakes

Aubret

2014

Heredity

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Island colonisation by animal populations is often associated with dramatic shifts in body size. However, little is known about the rates at which these evolutionary shifts occur, under what precise selective pressures and the putative role played by adaptive plasticity on driving such changes. Isolation time played a significant role in the evolution of body size in island Tiger snake populations, where adaptive phenotypic plasticity followed by genetic assimilation fine-tuned neonate body and head size (hence swallowing performance) to prey size. Here I show that in long isolated islands (46000 years old) and mainland populations, neonate body mass and snout-vent length are tightly correlated with the average prey body mass available at each site. Regression line equations were used to calculate body size values to match prey size in four recently isolated populations of Tiger snakes. Rates of evolution in body mass and snout-vent length, calculated for seven island snake populations, were significantly correlated with isolation time. Finally, rates of evolution in body mass per generation were significantly correlated with levels of plasticity in head growth rates. This study shows that body size evolution occurs at a faster pace in recently isolated populations and suggests that the level of adaptive plasticity for swallowing abilities may correlate with rates of body mass evolution. I hypothesise that, in the early stages of colonisation, adaptive plasticity and directional selection may combine and generate accelerated evolution towards an 'optimal' phenotype.

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“…The morphology of organisms is generally well matched to the environment, supposedly because expression of their genes is tailored at population or at individual level to suit local conditions (Aubret et al, 2004). Teixeira-Filho et al (2001) associated the use of different microhabitats, terrestrial occupation and occupation of smooth bromeliad leaf surfaces with variations in claw curvature of lizard species inhabiting restinga habitats.…”

Section: Introductionmentioning

confidence: 99%

Analysis of the microstructure of Xenodontinae snake scales associated with different habitat occupation strategies

Barbosa

2009

Braz. J. Biol.

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The morphology of many organisms seems to be related to the environment they live in. Nonetheless, many snakes are so similar in their morphological patterns that it becomes quite difficult to distinguish any adaptive divergence that may exist. Many authors suggest that the microornamentations on the scales of reptiles have important functional value. Here, we examined variations on the micromorphology of the exposed oberhautchen surface of dorsal, lateral, and ventral scales from the mid-body region of Xenodontinae snakes: Sibynomorphus mikani (terricolous), Imantodes cenchoa (arboreal), Helicops modestus (aquatic) and Atractus pantostictus (fossorial). They were metallized and analyzed through scanning electron microscopy. All species displayed similar microstructures, such as small pits and spinules, which are often directed to the scale caudal region. On the other hand, there were some singular differences in scale shape and in the microstructural pattern of each species. S. mikani and I. cenchoa have larger spinules arranged in a row which overlap the following layers on the scale surface. Species with large serrate borders are expected to have more frictional resistance from the caudal-cranial direction. This can favor life in environments which require more friction, facilitating locomotion. In H. modestus, the spinules are smaller and farther away from the posterior rows, which should help reduce water resistance during swimming. The shallower small pits found in this species can retain impermeable substances, as in aquatic Colubridae snakes. The spinules adhering to the caudal scales of A. pantostictus seem to form a more regular surface, which probably aid their fossorial locomotion, reducing scale-ground friction. Our data appear to support the importance of functional microstructure, contributing to the idea of snake species adaptation to their preferential microhabitats.Keywords: scales, microstructure, snakes, Xenodontinae, SEM. provavelmente auxilia na locomoção fossorial, reduzindo o atrito com o solo. Nossos dados parecem corroborar a importância da microestrutura funcional, contribuindo para a hipótese de adaptação das espécies de serpentes aos seus microhabitats preferenciais. Análise da microestrutura de escamas de serpentes Xenodontinae em associação à ocupação de diferentes microhabitatsPalavras-chave: escamas, microestrutura, serpentes, Xenodontinae, MEV.sisted of museum specimens from the Alphonse Richard Hoge collection at the Instituto Butantan (IB).In an attempt to avoid errors derived from phylogenetic factors, the species chosen all belong to the same subfamily (Xenodontinae).Dorsal, lateral and ventral scales were taken from the mid-region of the body of five adult individuals (males, 2 scales, and females, 3 scales) of each species. The scales were placed in numbered tubes and duly identified for each species. Distilled water and neutral soap were added to the tubes. Each tube was manually shaken for about 1 minute to remove any probable impurities. Scales were then removed...

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Adaptive developmental plasticity in snakes

Cited by 117 publications

References 5 publications

Adapting to an invasive species: Toxic cane toads induce morphological change in Australian snakes

Adapting to an invasive species: Toxic cane toads induce morphological change in Australian snakes

Island colonisation and the evolutionary rates of body size in insular neonate snakes

Analysis of the microstructure of Xenodontinae snake scales associated with different habitat occupation strategies

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