The evolution of vertebrate eye size across an environmental gradient: phenotype does not predict genotype in a Trinidadian killifish

Abstract

Vertebrates exhibit substantial variation in eye size. Eye size correlates positively with visual capacity and behaviors that enhance fitness, such as predator avoidance. This foreshadows a connection between predation and eye size evolution. Yet, the conditions that favor evolutionary shifts in eye size, besides the well-known role for light availability, are unclear. We tested the influence of predation on the evolution of eye size in Trinidadian killifish, Rivulus hartii. Rivulus are located across a series of communities where they coexist with visually oriented piscivores ("high predation" sites), and no predators ("Rivulus-only" sites). Wild-caught Rivulus from high predation sites generally exhibited a smaller relative eye size than communities that lack predators. Yet, such differences were inconsistent across rivers. Second-generation common garden reared fish revealed repeatable decreases in eye size in Rivulus from high predation sites. We performed additional experiments that tested the importance of light and resources on eye size evolution. Sites that differ in light or resource availability did not differ in eye size. Our results argue that differences in predator-induced mortality underlie genetically-based shifts in vertebrate eye size. We discuss the drivers of eye size evolution in light of the nonparallel trends between the phenotypic and common garden results.

Natural selection favours a larger eye in response to increased competition in natural populations of a vertebrate

“…That is, individuals with a larger relative eye size experience increased survival in both high‐predation and Rivulus‐ only localities (Figure ). Given these parallel trends across fish communities, the connection between eyes and survival does not appear to explain the locally adapted differences in eye size in Rivulus (Beston, Wostl, et al, ). However, we observed divergent relationships between eye size and rates of growth between high‐predation and Rivulus‐ only sites.…”

“…Eyes are energetically expensive organs (Laughlin, ; Moran, Softley, & Warrant, ), and we know that there is strong selection for maximal conversion of resources into somatic tissue in Rivulus‐ only sites (Walsh & Reznick, ) while high‐predation Rivulus instead invest heavily in reproduction (Walsh & Reznick, ). Larger eyes may enhance survival in high‐predation sites due to the improved detection of predators, but it is possible that the observed phenotypic divergence in this trait (Beston, Wostl, et al, ) is a reflection of higher food levels minimizing the need to invest in such a costly organ.…”

“…Indeed, studies have shown that ecological factors such as habitat complexity, foraging, diel activity and predation are associated with evolved differences in eye size (Banks, Sprague, Schmoll, Parnell, & Love, ; Beston, Dudycha, Post, & Walsh, in press; Beston, Wostl, & Walsh, ; Brandon, James, & Dudycha, ; Caves et al, ; Glazier & Deptola, ; Hammerschlag et al, ; Thomas et al, , ; Veilleux & Kirk, ; Zaret & Kerfoot, ). Although such studies provide information on the relationship between eye size and the environment, the vast majority of this work has compared eye size across species (but see Beston, Wostl, et al, ; Beston et al, in press; Brandon et al, ; Lönnstedt, McCormick, & Chivers, ). Despite years of research, very little work has experimentally tested how natural selection shapes the evolution of complex traits, such as the vertebrate eye.…”

“…We further evaluated the extent to which covarying shifts in light and resources explain the observed divergence in eye size between high‐predation and Rivulus‐ only sites using complementary comparisons. This approach showed that the presence (or absence) of predators, and not differences in light or food availability, best explains these evolved differences in eye size (Beston, Wostl, et al, ).…”

“…and Rivulus-only sites using complementary comparisons. This approach showed that the presence (or absence) of predators, and not differences in light or food availability, best explains these evolved differences in eye size (Beston, Wostl, et al, 2017).…”