Phenotypic plasticity (the ability of a single genotype to produce multiple phenotypes in response to variation in the environment) is commonplace. Yet its evolutionary significance remains controversial, especially in regard to whether and how it impacts diversification and speciation. Here, we review recent theory on how plasticity promotes: (i) the origin of novel phenotypes, (ii) divergence among populations and species, (iii) the formation of new species and (iv) adaptive radiation. We also discuss the latest empirical support for each of these evolutionary pathways to diversification and identify potentially profitable areas for future research. Generally, phenotypic plasticity can play a largely underappreciated role in driving diversification and speciation.

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Phenotypic plasticity's impacts on diversification and speciation

ECOLOGY/EVOLUTION: Phenotypic Plasticity

Nematode Parasites of Vertebrates: Their Development and Transmission

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Evolution In Changing Environments Some Theoretical Explorations

Phylogenetic studies of geographic range evolution are increasingly using statistical model selection methods to choose among variants of the dispersal-extinction-cladogenesis (DEC) model, especially between DEC and DEC+J, a variant that emphasizes “jump dispersal,” or founder-event speciation, as a type of cladogenetic range inheritance scenario. Unfortunately, DEC+J is a poor model of founder-event speciation, and statistical comparisons of its likelihood with DEC are inappropriate. DEC and DEC+J share a conceptual flaw: cladogenetic events of range inheritance at ancestral nodes, unlike anagenetic events of dispersal and local extinction along branches, are not modelled as being probabilistic with respect to time. Ignoring this probability factor artificially inflates the contribution of cladogenetic events to the likelihood, and leads to underestimates of anagenetic, time-dependent range evolution. The flaw is exacerbated in DEC+J because not only is jump dispersal allowed, expanding the set of cladogenetic events, its probability relative to non-jump events is assigned a free parameter, j, that when maximized precludes the possibility of non-jump events at ancestral nodes. DEC+J thus parameterizes the mode of speciation, but like DEC, it does not parameterize the rate of speciation. This inconsistency has undesirable consequences, such as a greater tendency towards degenerate inferences in which the data are explained entirely by cladogenetic events (at which point branch lengths become irrelevant, with estimated anagenetic rates of 0). Inferences with DEC+J can in some cases depart dramatically from intuition, e.g. when highly unparsimonious numbers of jump dispersal events are required solely because j is maximized. Statistical comparison with DEC is inappropriate because a higher DEC+J likelihood does not reflect a more close approximation of the “true” model of range evolution, which surely must include time-dependent processes; instead, it is simply due to more weight being allocated (via j) to jump dispersal events whose time-dependent probabilities are ignored. In testing hypotheses about the geographic mode of speciation, jump dispersal can and should instead be modelled using existing frameworks for state-dependent lineage diversification in continuous time, taking appropriate cautions against Type I errors associated with such methods. For simple inference of ancestral ranges on a fixed phylogeny, a DEC-based model may be defensible if statistical model selection is not used to justify the choice, and it is understood that inferences about cladogenetic range inheritance lack any relation to time, normally a fundamental axis of evolutionary models.

Conceptual and statistical problems with the DEC+J model of founder‐event speciation and its comparison with DEC via model selection

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.

Evolutionary biology: adaptive developmental plasticity in snakes.

https://www.cell.com/current-biology/pdf/S0960-9822(09)01775-8.pdf

Genetic Assimilation and the Postcolonization Erosion of Phenotypic Plasticity in Island Tiger Snakes

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 levels 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 suggests that mothers adjusted offspring phenotype to risky natal environments (tail length) or 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.

https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2014.0701

Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal

http://www.kingsnake.com/aho/pdf/November2003Update/aubret2002.pdf

Fat is sexy for females but not males: the influence of body reserves on reproduction in snakes (Vipera aspis).

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 degrees C), intermediate (19-26 degrees C) or hot (19-37 degrees 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).

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Fabien Aubret

Papers

Evolutionary biology: adaptive developmental plasticity in snakes.

Genetic Assimilation and the Postcolonization Erosion of Phenotypic Plasticity in Island Tiger Snakes

Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal

Fat is sexy for females but not males: the influence of body reserves on reproduction in snakes (Vipera aspis).

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