Parallel phenotypes underpinned by different genes in the visual system of two trans-isthmian coral reef fish species pairs

Abstract

Understanding the genetic basis of adaptation in natural populations to changing environmental conditions is challenging. The relatively simple genotype-to-phenotype relationship between opsin genes and visual pigments offers a particularly informative model to explore the molecular mechanisms underpinning adaptive phenotypic change in natural populations. Here we leveraged the natural experiment provided by the tectonic closure of the Central American seaway that created allopatric, sister taxa in multiple, independent lineages of marine organisms and exposed them to distinct underwater light environments: either the more turbid Tropical Eastern Pacific (TEP), or the spectrally broader Caribbean Sea. Using two species pairs of planktivorous teleosts, the Azurina multilineata/A. atrilobata damselfish and the Cephalopholis (Paranthias) furcifer/C. colonus groupers, we explore to what extent visual sensitivity converged to similar adaptations in response to similar foraging strategies and shared underwater light in each marine basin. We found that the compression of the underwater light field towards the central portion of the spectrum from Caribbean to TEP waters is reflected in similar shifts towards the centre of the light spectrum in overall single and double cone sensitivities in both families. Both TEP species have single (short-wavelength) cone sensitivities shifted to longer wavelengths and double (long-wavelength) cone sensitivities shifted to shorter wavelengths, compared to their Caribbean counterparts. These parallel shifts in visual sensitivities observed in response to shared underwater light environments are accomplished by different underlying opsin gene toolsets in the two lineages. Similarly, expression changes in pathways associated with the visual system revealed limited parallelism at the molecular level.