How plasticity, genetic assimilation and cryptic genetic variation may contribute to adaptive radiations

Abstract

There is increasing evidence that phenotypic plasticity can promote population divergence by facilitating phenotypic diversification and, eventually, genetic divergence. When a 'plastic' population colonizes a new habitat, it has the possibility to occupy multiple niches by expressing several distinct phenotypes. These initially reflect the population's plastic range but may later become genetically fixed by selection via the process of 'genetic assimilation' (GA). Through this process multiple specialized sister lineages can arise that share a common plastic ancestor - the 'flexible stem'. Here, we review possible molecular mechanisms through which natural selection could fix an initially plastic trait during GA. These mechanisms could also explain how GA may contribute to cryptic genetic variation that can subsequently be coopted into other phenotypes or traits, but also lead to nonadaptive responses. We outline the predicted patterns of genetic and transcriptional divergence accompanying flexible stem radiations. The analysis of such patterns of (retained) adaptive and nonadaptive plastic responses within and across radiating lineages can inform on the state of ongoing GA. We conclude that, depending on the stability of the environment, the molecular architecture underlying plastic traits can facilitate diversification, followed by fixation and consolidation of an adaptive phenotype and degeneration of nonadaptive ones. Additionally, the process of GA may increase the cryptic genetic variation of populations, which on one hand may serve as substrate for evolution, but on another may be responsible for nonadaptive responses that consolidate local allopatry and thus reproductive isolation.

Adaptive phenotypic plasticity contributes to divergence between lake and river populations of an East African cichlid fish

“…Cichlid species that show phenotypic plasticity are often riverine or a part of very recent intralacustrine adaptive radiations (Greenwood, 1964; Meyer, 1989; Smits et al., 1996; Chapman, Galis, & Shinn, 2000) and riverine species show the highest level of adaptive plasticity among the East African cichlids investigated so far, lending support to the ‘flexible stem hypothesis’ (Schneider & Meyer, 2017). If temporal and/or spatial variation is higher in river than in lake habitat, plasticity would be favored over genetic divergence (Scheiner, 1993; Sultan & Spencer, 2002).…”

“…Plastic lineages can persist in a new habitat, even if there are no similar niches available, and are therefore expected to have higher potential for adaptive diversification than nonplastic lineages (Schneider & Meyer, 2017). In stickleback, transcriptomic plasticity may play a substantial role in migrants’ adaptation to novel environments (Lohman et al., 2017).…”

“…However, there is growing evidence that under certain conditions, genotypic variability and phenotypic plasticity are complementary mechanisms that jointly facilitate adaptation, speciation and even adaptive radiation (for reviews see: Price, Qvarnstrom, & Irwin, 2003; West‐Eberhard, 2003; Pfennig et al., 2010; Schneider & Meyer, 2017). …”

Understanding the molecular basis of adaptation to freshwater environments by prawns in the genus Macrobrachium

“…Colonization of freshwater from a marine ancestral state represents a major evolutionary transition, in which phenotypic plasticity plasticity (ability of a single genotype to produce variable phenotypes in different environments) which is widespread in nature, is likely to have played a vital role, following which plasticity itself may be subject to adaptive processes (Orr, 2005;Gibbons et al, 2017;Schneider and Meyer, 2017). A variety of changes potentially occur in plastic responses following freshwater colonization.…”

“…Plastic responses however, can also be deleterious if they shift phenotypes from the optimum range so that organisms are unable to buffer against perturbations imposed by the newly colonized environment (Scheiner, 1993;Huang and Agarwal, 2016). In general, phenotypic plasticity can offer advantages to organisms that inhabit heterogeneous environments by potentially allowing them to increase their geographical ranges, enhance persistence, and/or relative fitness (Schneider and Meyer, 2017).…”