Convergent phenotypic evolution of the visual system via different molecular routes: How Neotropical cichlid fishes adapt to novel light environments.

Andreas Härer,Julián Torres-Dowdall,Axel Meyer

doi:10.1002/evl3.71

Andreas Härer, Julián Torres-Dowdall + Show 1 more

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https://doi.org/10.1002/evl3.71

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Abstract

How predictable is evolution? This remains a fundamental but contested issue in evolutionary biology. When independent lineages colonize the same environment, we are presented with a natural experiment that allows us to ask if genetic and ecological differences promote species‐specific evolutionary outcomes or whether species phenotypically evolve in a convergent manner in response to shared selection pressures. If so, are the molecular mechanisms underlying phenotypic convergence the same? In Nicaragua, seven species of cichlid fishes concurrently colonized two novel photic environments. Hence, their visual system represents a compelling model to address these questions, particularly since the adaptive value of phenotypic changes is well‐understood. By analyzing retinal transcriptomes, we found that differential expression of genes responsible for color vision (cone opsins and cyp27c1) produced rapid and mostly convergent changes of predicted visual sensitivities. Notably, these changes occurred in the same direction in all species although there were differences in underlying gene expression patterns illustrating nonconvergence at the molecular level. Adaptive phenotypes evolved deterministically, even when species differ substantially in ecology and genetic variation. This provides strong evidence that phenotypic evolution of the visual system occurred in response to similar selective forces of the photic environment.

Highlights

Almost 30 years ago, the famous paleontologist and evolutionary biologist Stephen J
Quantitative Real-Time PCR and in situ hybridization analyses showed that crater lake Midas cichlids (Amphilophus cf. citrinellus) have a short wavelength shifted visual system compared to one source population from the great lakes (Torres-Dowdall et al 2017)
H. nematopus and P. managuensis, two species with extremely different ecologies (Table S1), changed visual phenotypes in parallel across river, great lake, and crater lake in a way that maintained interspecific differences in each of these environments (Fig. 3C). Even though both species shifted their vision to absorb more short wavelength light in the crater lake compared to the river, the riverine population of H. nematopus still has a shorter wavelength shifted sensitivity than P. managuensis from the crater lake. These results strongly suggest that overall photic environment and ecological characteristics of the species both influence color vision, which is in agreement with existing knowledge on adaptive evolution of the visual system (Cronin et al 2014)

Summary

Introduction

Almost 30 years ago, the famous paleontologist and evolutionary biologist Stephen J. Examples of convergence are the repeated loss of armor plates in threespine sticklebacks (Colosimo et al 2005), changes in body shape in Anolis lizards (Mahler et al 2013), threespine sticklebacks (Schluter and McPhail 1992; Rundle et al 2000) and cichlid fishes (Meyer 1990; Elmer et al 2010a; Elmer et al 2014) and life-history evolution in guppies (Reznick and Endler 1982; Reznick et al 1996) These cases, in which populations of the same, or closely related species, independently colonized similar environments and predictably and repeatedly diverged from the ancestral state have provided valuable insights into how adaptive evolution proceeds. A compelling, but less frequently applied approach is to study convergent evolution of certain phenotypic traits in lineages that concurrently colonized the same environment (Rosenblum 2006; Rosenblum et al 2017)

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