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

Abstract

Eye size varies notably across taxa. Much work suggests that this variation is driven by contrasting ecological selective pressures. However, evaluations of the relationship between ecological factors and shifts in eye size have largely occurred at the macroevolutionary scale. Experimental tests in nature are conspicuously absent. Trinidadian killifish, Rivulus hartii, are found across fish communities that differ in predation intensity. We recently showed that increased predation is associated with the evolution of a smaller eye. Here, we test how divergent predatory regimes alter the trajectory of eye size evolution using comparative mark–recapture experiments in multiple streams. We found that increases in eye size are associated with enhanced survival, irrespective of predation intensity. More importantly, eye size is associated with enhanced growth in communities that lack predators, while this trend is absent when predators are present. Such results argue that increased competition for food in sites that lack predators is the key driver of eye size evolution. A plain language summary is available for this article.

Coordinated evolution of brain size, structure, and eye size in Trinidadian killifish

“…The connection between brain structures and eye size is also potentially adaptive. Previous work in killifish has shown that increases in eye size are associated with greater survival and enhanced growth in sites that lack predators (Beston & Walsh, 2019). This suggests that the increased competition for food in RO sites selects for increased eye size and that brain structures may evolve as an indirect byproduct.…”

“…Evolutionary shifts in eye size have also been linked to changes in ecological conditions. For example, studies have quantified selection on eye size due to such factors as light availability (Hall, 2008; Hiller‐Adams & Case, 1988; Kröger & Fernald, 1994; Veilleux & Lewis, 2011), predation (Glazier & Deptola, 2011; Møller & Erritzøe, 2010; Nilsson et al., 2012), and competition (Beston et al., 2017, 2019; Beston & Walsh, 2019). This growing body of work illustrating similar shifts in brain and eye size in response to ecologically mediated selection foreshadows the possibility that selection favors coordinated shifts in these neurosensory systems.…”

“…These trends were maintained after two generations of common garden rearing, which indicates that these differences are likely genetically based (Walsh et al., 2016). Similarly, male killifish from RO sites have also evolved a larger relative eye size than males from high predation sites (Beston & Walsh, 2019; Beston et al., 2017). These evolved differences in brain and eye size between sites with and without predators present the opportunity to determine whether increased predation has also driven shifts in brain architecture and whether there is a coordinated pattern of evolution among brain size, brain structure, and eye size.…”

More than meets the eye: Predator‐induced pupil size plasticity in a teleost fish

“…Recent studies have linked selection for large eye/pupil size to e.g. dim light habitats and nocturnal behaviour (Martinez‐Ortega, Santos, & Gil, 2014; Schmitz & Wainwright, 2011; Warrant, 2004) or to competition (Beston & Walsh, 2019) and predation risk per se (Freund & Olmstead, 2000; Glazier & Deptola, 2011; Møller & Erritzoe, 2010; Nilsson et al., 2012). Such changes may be of particular importance in the many teleost fish that lack a pupillary sphincter muscle and, hence, have a pupil that is fixed in size and not responsive to ambient light intensity (Douglas, 2018; Helfman et al., 2009).…”

“…An increase in nocturnality may thus select for facultative and rapid adaptations of the visual system, enabling night‐time activity. Such changes in diel rhythms have recently been suggested as the selective agent driving evolutionary shifts in eye size among populations of the Trinidadian killifish Rivulus hartii (Beston & Walsh, 2019). Furthermore, a recent study demonstrated that selection pressures on activity patterns have been the main drivers for evolutionary divergence in the mammalian eye (Baker & Venditti, 2019).…”