Towards a gene regulatory network perspective on phenotypic plasticity, genetic accommodation and genetic assimilation

Many organisms can produce alternative phenotypes in direct response to different environmental conditions, a phenomenon known as phenotypic plasticity. The environmentally sensitive gene regulatory networks (GRNs) that mediate such developmental flexibility are largely unknown. Yet, characterizing these GRNs is important not only for elucidating plasticity’s molecular basis, but also for shedding light onto whether and how plasticity might impact evolution. In this issue of Molecular Ecology, Schneider et al.) describe one of the first efforts to determine the GRN underlying a plastic trait. They focus on diet-induced plasticity in the cichlid fish, Astatoreochromis alluaudi. Depending on whether soft food (e.g. insects) or hard food (e.g. molluscs) is consumed, this species forms a lower pharyngeal jaw (LPJ) with many fine teeth or with fewer molar-like teeth, respectively (Fig. 1). The authors previously identified genes that are differentially expressed between LPJ morphs during early development. In the present study, they examine the expression of 19 of these genes across development and diet. By analysing these transcriptional data in combination with information on putative transcription factor binding sites, they construct a GRN that explains observed gene expression patterns and is likely to control LPJ morphology. This work advances our understanding of how plasticity can arise as a consequence of environmentally sensitive GRNs and promises to help illuminate how changes in such GRNs could facilitate evolution. Fig. 1 The cichlid fish, Astatoreochromis alluaudi, exhibits diet-induced plasticity in the morphology of its lower pharyngeal jaw. Keywords: adaptation, fish, gene regulatory networks, macroevolution, molecular evolution, phenotypic plasticity The flexible organism Among evolutionary biology’s central challenges is to explain why there are so many different species and where their distinctive traits come from. Phenotypic plasticity is increasingly viewed as playing a crucial role in both diversification and innovation (West-Eberhard 2003). When selection acts on quantitative genetic variation regulating the expression of an environmentally induced trait, it can promote the evolution of either increased or decreased plasticity through an evolutionary process known as ‘genetic accommodation’ (sensu West-Eberhard 2003). If the affected trait evolves decreased plasticity to the point of becoming constitutively expressed, ‘genetic assimilation’ occurs (sensu Waddington 1953). Through this process – in which a novel, complex trait evolves from a trait that was originally induced by the environment – new traits and possibly even new species can emerge (Pfennig et al. 2010). Yet, little is known about whether and how genetic accommodation/assimilation shape ecologically and evolutionarily relevant traits in natural populations (Pfennig et al. 2010). East African cichlids are ideal for studying genetic accommodation/assimilation. This group is renowned both for its spectacular species richness (there are over 500 species in Lake Victoria alone) and for its stunning array of highly specialized feeding morphologies (Seehausen 2006). Indeed, this impressive diversity is thought to stem (in part) from the cichlid’s ability to rapidly evolve specializations for utilizing diverse feeding niches: these fish possess a versatile pharyngeal jaw, which has been modified repeatedly to exploit different resource (Liem 1974). One recent hypothesis holds that the cichlid adaptive radiation arose when ecological circumstances favoured diversification in ancestral lineages that possessed a phenotypically plastic pharyngeal jaw; later, this flexible jaw repeatedly underwent genetic assimilation to produce the present-day diversity among species in feeding morphologies (West-Eberhard 2003). Astatoreochromis alluaudi is well suited for testing this hypothesis. This species is a dietary generalist, ancestral to modern East African cichlids. Moreover, it exhibits diet-induced phenotypic plasticity in its lower pharyngeal jaw (LPJ). If its preferred diet of soft food (e.g. insects) is present, A. alluaudi develops a slender ‘papilliform’ LPJ, bearing numerous fine teeth. However, if soft food is scarce, individuals feed on hard-shelled molluscs, which induces formation of a robust ‘molariform’ LPJ, bearing fewer, molar-like teeth (Fig. 1). Thus, LPJ plasticity in A. alluaudi represents a valuable model for examining how phenotypic plasticity might have contributed to the diversity of jaw morphologies among East African cichlids.