A pleiotropic interaction between vision loss and hypermelanism in Astyanax mexicanus cave x surface hybrids

Abstract

BackgroundCave-dwelling animals evolve various traits as a consequence of life in darkness. Constructive traits (e.g., enhanced non-visual sensory systems) presumably arise under strong selective pressures. The mechanism(s) driving regression of features, however, are not well understood. Quantitative trait locus (QTL) analyses in Astyanax mexicanus Pachón cave x surface hybrids revealed phenotypic effects associated with vision and pigmentation loss. Vision QTL were uniformly associated with reductions in the homozygous cave condition, however pigmentation QTL demonstrated mixed phenotypic effects. This implied pigmentation might be lost through both selective and neutral forces. Alternatively, in this report, we examined if a pleiotropic interaction may exist between vision and pigmentation since vision loss has been shown to result in darker skin in other fish and amphibian model systems.ResultsWe discovered that certain members of Pachón x surface pedigrees are significantly darker than surface-dwelling fish. All of these “hypermelanic” individuals demonstrated severe visual system malformations suggesting they may be blind. A vision-mediated behavioral assay revealed that these fish, in stark contrast to surface fish, behaved the same as blind cavefish. Further, hypermelanic melanophores were larger and more dendritic in morphology compared to surface fish melanophores. However, hypermelanic melanophores responded normally to melanin-concentrating hormone suggesting darkening stemmed from vision loss, rather than a defect in pigment cell function. Finally, a number of genomic regions were coordinately associated with both reduced vision and increased pigmentation.ConclusionsThis work suggests hypermelanism in hybrid Astyanax results from blindness. This finding provides an alternative explanation for phenotypic effect studies of pigmentation QTL as stemming (at least in part) from environmental, rather than exclusively genetic, interactions between two regressive phenotypes. Further, this analysis reveals persistence of background adaptation in Astyanax. As the eye was lost in cave-dwelling forms, enhanced pigmentation resulted. Given the extreme cave environment, which is often devoid of nutrition, enhanced pigmentation may impose an energetic cost. Such an energetic cost would be selected against, as a means of energy conservation. Thus, the pleiotropic interaction between vision loss and pigmentation may reveal an additional selective pressure favoring the loss of pigmentation in cave-dwelling animals.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0716-y) contains supplementary material, which is available to authorized users.

Phenotypic plasticity as a mechanism of cave colonization and adaptation

“…The increase in melanophores in darkraised SF was modest and confined to specific regions of the body, but consistent with upregulation of some melanosome-related genes in the transcriptome. This result was unexpected but considered reliable, since SF x CF hybrids can also show hyper-melanization [65], and neutral mutations are a likely cause of melanophore reduction in A. mexicanus CF [66]. We found a surprising result in another classic troglomorphic trait, eye degeneration: although visual perception was a GO term associated with down-regulated DEGs in D/D SF transcriptome, we were unable to detect changes in eye size.…”

The Integrated Genomic Architecture and Evolution of Dental Divergence in East African Cichlid Fishes (Haplochromis chilotes x H. nyererei)

“…For instance, the capacity of the two jaws of cichlid fishes to evolve independently has been commonly invoked as a critical catalyst underlying both the unparalleled trophic divergence of these fishes and the phenomenal convergence that characterizes their adaptive radiations ( Liem 1973 ; Hulsey et al 2006 ). However, the degree to which particular parts of phenotypes can evolve independently and contribute to adaptation might be largely a result of their underlying genetic architectures ( Lande 1984 ; Albertson and Kocher 2006 ; Brakefield 2006 ; Wilkens 2010 ; Albertson et al 2014 ; Armbruster et al 2014 ; Gross et al 2016 ). Structures ranging from flower pistils to snake vertebrae to primate teeth have been suggested to evolve largely according to their genetic covariance ( Schluter 1996 ; Hohenlohe and Arnold 2008 ; Hlusko 2016 ; Smith 2016 ).…”

Genetic analysis reveals candidate genes for activity QTL in the blind Mexican tetra,Astyanax mexicanus

“…Fish used in these studies were part of a laboratory population maintained at the University of Cincinnati. All specimens were laboratory-bred Astyanax mexicanus belonging to lines originally sourced from the Sierra de El Abra region of northeastern Mexico ( Gross et al, 2016a ; Gross et al, 2016b ). F 1 and F 2 hybrids were generated by crossing male surface fish with female (Pachón) cavefish.…”