A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems

Abstract

A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation arises and is sorted by natural selection. Here we argue that an integrated view, which merges ecology, evolution and developmental biology (eco evo devo) on an equal footing, is needed to understand the multifaceted role of the environment in simultaneously determining the development of the phenotype and the nature of the selective environment, and how organisms in turn affect the environment through eco evo and eco devo feedbacks. To illustrate the usefulness of an integrated eco evo devo perspective, we connect it with the theory of resource polymorphism (i.e. the phenotypic and genetic diversification that occurs in response to variation in available resources). In so doing, we highlight fishes from recently glaciated freshwater systems as exceptionally well‐suited model systems for testing predictions of an eco evo devo framework in studies of diversification. Studies on these fishes show that intraspecific diversity can evolve rapidly, and that this process is jointly facilitated by (i) the availability of diverse environments promoting divergent natural selection; (ii) dynamic developmental processes sensitive to environmental and genetic signals; and (iii) eco evo and eco devo feedbacks influencing the selective and developmental environments of the phenotype. We highlight empirical examples and present a conceptual model for the generation of resource polymorphism – emphasizing eco evo devo, and identify current gaps in knowledge.

“And if you gaze long into an abyss, the abyss gazes also into thee”: four morphs of Arctic charr adapting to a depth-gradient in Lake Tinnsjøen

“…Although the Arctic charr species complex has been studied for a long time, researchers still need to address the important mechanisms underlying origin, presence and temporal persistence of sympatric morphs. Thus, a multi-method based eco-evo-devo approach with ecological, morphological and life history studies [146], and state of the art genomics as performed in Lake Tingvallavatn [e.g. 144, 145], seem to be a good avenue, as well as the methods applied in Jacobs et al [23] contrasting two independent replicate lineage radiations of the Arctic charr.…”

Does phenotypic plasticity initiate developmental bias?

“…Could this lack of expansion into truly novel niches be due to biases in phenotypic plasticity? For damselfish, we are unaware of research suggesting plasticity in trophic morphology but would expect that they follow patterns of responses found across a wide range of fish species (Parsons et al, 2016;Robinson & Parsons, 2002;Skúlason et al, 2019). These plastic responses are likely adaptive based on well-established relationships in Anolis including among populations of some species and among species (Irschick & Losos, 1998;Losos & Irschick, 1996).…”

“…In many ways, plasticity is now seen as a conventional trait possessing heritable variation that is widely evident among the reaction norms of different clonal lines and across populations (Pigliucci, 2006;Skúlason et al, 2019). In many ways, plasticity is now seen as a conventional trait possessing heritable variation that is widely evident among the reaction norms of different clonal lines and across populations (Pigliucci, 2006;Skúlason et al, 2019).…”

A phenotypically plastic magic trait promoting reproductive isolation in sticklebacks?

“…Although evidence of such traits in nature is sparse (Servedio et al 2011), magic traits are usually envisaged as inherited and linked to mate choice through pleiotropy. However, much research interest has focused on the possible role of phenotypic plasticity in the initiation of evolutionary change through the development of discrete alternative phenotypes (West-Eberhard 1989, 2003Fitzpatrick 2012;Skulason et al 2019). If expressed alternative phenotypic traits induced by the environment through plasticity, also form part of the mate choice system of the diverging organism, then assortative mating resulting from mate choice based on such traits have the potential to generate reproductive barriers between individuals expressing different phenotypes (Fitzpatrick 2012).…”