Ontogeny and evolution: parallel cooption of developmental pathways in the adaptive evolution of the visual system of Neotropical cichlid fish in recently colonized crater lakes

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Understanding the factors affecting biological change is an ultimate goal in evolutionary biology, even more crucial now in the face of global change. However, the predictability of evolution is a contested topic. Some authors argue that stochastic factors are predominant, and thus, biological change is inherently unpredictable. Others see in the many cases of parallel evolution the deterministic signature of natural selection. The presence of similar adaptive peaks in the fitness landscape is the potential cause of parallelisms, but not necessarily their only explanation. Common genomic backgrounds and developmental constraints among closely related species might also affect the direction of biological change, in which case, genetic parallelisms are expected to underlie parallel phenotypic evolution. Here, I aim to determine if parallel phenotypic evolution of closely related species is underpinned by genetic parallelisms originating from the cooption of common developmental pathways. I propose to study the adaptive evolution of visual sensitivity in Nicaraguan Midas cichlid fishes. This species flock offers a natural experiment to address this topic because multiple clear crater lakes with similar light conditions were independently colonized from turbid great lakes, their radiation occurred recently resulting in little genomic divergence, and their phylogenetic relationships are well understood. The visual sensitivity of Midas cichlids has evolved rapidly and in parallel after the colonization of the crater lakes from the great lakes. Also, the visual sensitivity of the derived crater lake species resembles that in juveniles from the ancestral great lakes. Thus, I hypothesize that 1) developmental pathways were coopted during adaptive evolution to the novel conditions and, hence, 2) a high degree of parallelism in the underlying molecular mechanisms is expected among crater lake lineages. An approach combining forward and reverse genetics will be used to empirically test these hypotheses. First, I will test retinal transcriptomes for a positive association between differentially expressed genes underlying evolutionary divergence (i.e., crater vs. great lakes) and those underlying ontogenetic changes in the ancestral population (i.e., great lakes) as predicted by the first hypothesis. The second hypothesis predicts those genes to be the same in the species from different crater lakes. Then, I will study the genetic architecture of visual sensitivity by eQTL analyses in two independent ancestral-derived hybrid crosses. Common genomic regions are expected to underlie parallel changes in expression of genes affecting visual sensitivity in both crosses. Finally, I will use genomic editing to functionally challenge the identified loci. This project adds to the longstanding debate about the predictability of evolution and will further our understanding of the mechanisms involved in development and adaptive divergence in visual sensitivity.