Ancestral variation and the potential for genetic accommodation in larval amphibians: implications for the evolution of novel feeding strategies

Abstract

Few studies provide empirical evidence for phenotypic plasticity's role in the evolution of novel traits. One way to do so is to test whether latent plasticity is present in an ancestor that can be refined, enhanced, or diminished by selection in derived taxa (through "genetic accommodation"), thereby producing novel traits. Here, we evaluated whether gut plasticity preceded and promoted the evolution of a novel feeding strategy in spadefoot toad tadpoles. We studied Scaphiopus couchii, whose tadpoles develop an elongate gut and consume only detritus, and two derived species, Spea multiplicata and Sp. bombifrons, whose tadpoles also express a novel, short-gut phenotype in response to a novel resource (anostracan shrimp). Consistent with the expectations of plasticity-mediated trait evolution, we found that shrimp induced a range of phenotypes in Scaphiopus that were not produced with detritus. This plasticity was either suppressed or exaggerated in Spea depending on whether the induced phenotypes were adaptive. Moreover, in contrast to its effects on morphology, shrimp induced little or no functional plasticity, as assessed by gut cell proliferation, in Scaphiopus. Shrimp did, however, induce substantial proliferation in Sp. bombifrons, the species that consumes the most shrimp and that produces the short-gut phenotype the most frequently. Thus, if Spea had ancestral morphological plasticity in response to a novel diet, their shrimp-induced short-gut morphology may have undergone subsequent genetic accommodation that improved its functionality. Hence, diet-induced phenotypic plasticity may have preceded and even promoted the evolution of a novel phenotype.

Evolution of adaptive phenotypic traits without positive Darwinian selection

“…Similarly, in spadefoot toads (Spea sp.) there is evidence that phenotypic plasticity with respect to larval diet and gut morphology preceded the evolution of species whose larvae showed a greater tendency toward carnivory (Ledon-Rettig et al, 2008). Similarly, there is evidence that phenotypic plasticity preceded evolution of morphologically distinct ecotypes in threespine sticklebacks Gasterosteus aculeatus (Wund et al, 2008).…”

Extinction or Survival? Behavioral Flexibility in Response to Environmental Change in the African Striped Mouse Rhabdomys

“…Although similar to inherent resilience, in adaptive resilience, gene expression is relaxed and facultative based on prevailing environmental conditions [32]. For example, in spade foot toad Scaphiopus species, tadpoles develop into one of two morphs: carnivore morphs feeding on shrimps develop a short gut whereas omnivores feeding on detritus have longer guts [34].…”

Developmental plasticity and evolution—quo vadis?

“…Similarly, across phyla gut formation is responsive to dietary conditions, which in turn delineates which future dietary environments the developing organism will experience (Ledón-Rettig et al 2008;Bloom et al 2013;Christeller et al 2010;Saikia et al 2011;Agrawal et al 2002). In these and many other cases, plastic responses to environmental conditions often do not simply adjust aspects of phenotype formation but also modify the selective environmental conditions in which the developing organism finds itself.…”

“…Instead, plasticity research may benefit from (re) emphasizing more strongly that plasticity may be best understood as an emergent property of developmental systems, and one that is enabled by diverse biological mechanisms, at least some of which may not primarily be underlain by differential gene expression or affected by sequence variation. Interestingly, efforts to adopt such a developmental systems perspective have led to some of the most significant recent progress in both the search for the developmental causes of disease (for example, Barker, 2013;McMullen and Swali, 2013) and the developmental basis of major evolutionary transitions (for example, Ledón-Rettig et al 2008Standen et al 2014), and there is every reason to believe that such an integrative approach could be similarly advantageous for research programs in developmental plasticity.…”