Sexual selection and the evolution of the vertebrate visual system

What explains variation in female preference?  This classic question in sexual selection has important implications for evolutionary theory and the generation of biodiversity. The guppy and closely related species in the family Poeciliidae comprise one of the best models for studying this question.  In the past several years, we have described the tuning of the peripheral visual system in various habitats and species in order to address one critical aspect of this overall question: at what level of biological organization do differences in preference behaviour arise?  We have concentrated on the long wave-sensitive (LWS) opsins, given that female guppies are strongly attracted to orange and red male coloration. We intend to expand our examination of the environmental and genetic causes of variation in the tuning of the peripheral visual system, and also ask how do higher order neural processes control preference?  Our main effort in this new area will be to examine variation in gene expression in the brains of females experiencing different visual environments. 

Genetic and genomic variation for color opsin genes 

Variation in color vision is often driven by duplication of opsin genes, or variation in a few key amino acids. Our studies showed remarkably little genetic or genomic variation across 14 species of Poeciliids. This information also allowed the development of locus-specific primers that have been adopted by several labs. (bold denotes graduate student, italics undergraduate trainee). Watson, et al. 2010. Genomic organization of duplicated short wave-sensitive and long wave-sensitive opsin genes in the green swordtail, Xiphophorus helleri. BMC Evolutionary Biology 10:87. Watson, Sandkam, et al. 2011. Gene duplication and divergence of long wavelength-sensitive opsin genes in the guppy, Poecilia reticulata.  Journal of Molecular Evolution 72:240–252. Sandkam, Watson, et al. (in review) Genomic environment impacts color vision evolution in a family with visually-based sexual selection.  Genome Biology and Evolution.

Environmental and Genetic control of opsin expression 

Given the lack of genetic and genomic variation in LWS opsin genes, we asked whether variation in level of expression of color opsins could control preferences.  We started with guppies from high- and low-predation Trinidadian streams, a powerful system for studying evolution by sexual selection.  In a high impact study, we showed that LWS expression was elevated in upstream populations, where females express much stronger preference for orange/red males (this paper was the cover article, and ranks in the top 5% in Molecular Ecology based on an altmetric score that reflects reads and social media attention). This study also showed that one amino acid polymorphism that shifts LWS color sensitivity correlates with upstream/downstream habitats. Sandkam, Young et al.  2015. Beauty in the eyes of the beholders: Color vision is tuned to mate preference in the Trinidadian guppy (Poecilia reticulata).  Molecular Ecology 24:596-609.

We expanded this analysis to multiple species in Guyana, because several species occur in the same habitats, making it a powerful system to examine the effect of environmental versus genetic effects on opsin expression.   Both expression and allelic variation was highly similar within streams, suggesting strong environmental control. Sandkam, Young, Breden, F. M. W. et al. 2015. Color vision varies more among populations than among species of live-bearing fish from South America. BMC Evolutionary Biology 15:225.

By testing guppies raised in turbid and non-turbid environments, we were able to experimentally show strong effects of environment on opsin gene expression. Ehlman, Sandkam et al. 2015. Developmental plasticity in vision and behavior may help guppies overcome increased turbidity. Journal of Comparative Physiology A 201:1125-1135.

We discovered a highly conserved locus-control region upstream of LWS tandem repeats that can change gene expression by two orders of magnitude, and this will be very important in our future studies of the genetic control of opsin gene expression. Tam, Watson, et al. 2011. Regulatory function of conserved sequences upstream of the long-wave sensitive opsin genes in teleost fishes. Vision Research 51: 2295-2303.

Summary: This set of studies is rare in sexual selection, in that we were able to examine many environmental factors across multiple populations and species for a class of molecules, opsins, for which it is possible to go from allelic variation and expression, to changes in physiology (tuning of the retina) to behavior (testing for changes in female preferences).  We have observed: a high proportion of the variation is driven by the environment rather than genetic differences among species, a high level of variation in opsin expression among environments, and this was correlated with female preference differences in Trinidad.


Figure 1. Complete description of LWS and SWS2 genomic repertoire for the green swordtail, Xiphpophorus helleri. This is the first full description of LWS and SWS2 genes for any livebearing fish, and shows the tail to tail orientation of two of the tandem repeats.