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

Brain size, brain architecture, and eye size vary extensively in vertebrates. However, the extent to which the evolution of these components is intricately connected remains unclear. Trinidadian killifish, Anablepsoides hartii, are found in sites that differ in the presence and absence of large predatory fish. Decreased rates of predation are associated with evolutionary shifts in brain size; males from sites without predators have evolved a relatively larger brain and eye size than males from sites with predators. Here, we evaluated the extent to which the evolution of brain size, brain structure, and eye size covary in male killifish. We utilized wild-caught and common garden-reared specimens to determine whether specific components of the brain have evolved in response to differences in predation and to determine if there is covariation between the evolution of brain size, brain structure, and eye size. We observed consistent shifts in brain architecture in second generation common garden reared, but not wild caught preserved fish. Male killifish from sites that lack predators exhibited a significantly larger telencephalon, optic tectum, cerebellum, and dorsal medulla when compared with fish from sites with predators. We also found positive connections between the evolution of brain structure and eye size but not between overall brain size and eye size. These results provide evidence for evolutionary covariation between the components of the brain and eye size. Such results suggest that selection, directly or indirectly, acts upon specific regions of the brain, rather than overall brain size, to enhance visual capabilities.

Predation drives the evolution of brain cell proliferation and brain allometry in male Trinidadian killifish, Rivulus hartii.

The external environment influences brain cell proliferation, and this might contribute to brain plasticity underlying adaptive behavioural changes. Additionally, internal genetic factors influence the brain cell proliferation rate. However, to date, researchers have not examined the importance of environmental versus genetic factors in causing natural variation in brain cell proliferation. Here, we examine brain cell proliferation and brain growth trajectories in free-living populations of Trinidadian killifish, Rivulus hartii, exposed to contrasting predation environments. Compared to populations without predators, populations in high predation (HP) environments exhibited higher rates of brain cell proliferation and a steeper brain growth trajectory (relative to body size). To test whether these differences in the wild persist in a common garden environment, we reared first-generation fish originating from both predation environments in uniform laboratory conditions. Just as in the wild, brain cell proliferation and brain growth in the common garden were greater in HP populations than in no predation populations. The differences in cell proliferation observed across the brain in both the field and common garden studies indicate that the differences are probably genetically based and are mediated by evolutionary shifts in overall brain growth and life-history traits.

The evolution of eye size in response to increased fish predation in Daphnia.

Variation in eye size is ubiquitous across taxa. Increased eye size is correlated with improved vision and increased fitness via shifts in behavior. Tests of the drivers of eye size evolution have focused on macroevolutionary studies evaluating the importance of light availability. Predator-induced mortality has recently been identified as a potential driver of eye size variation. Here, we tested the influence of increased predation by the fish predator, the alewife (Alosa pseudoharengus) on eye size evolution in waterfleas (Daphnia ambigua) from lakes in Connecticut. We quantified the relative eye size of Daphnia from lakes with and without alewife using wild-caught and third-generation laboratory reared specimens. This includes comparisons between lakes where alewife are present seasonally (anadromous) or permanently (landlocked). Wild-caught specimens did not differ in eye size across all lakes. However, third-generation lab reared Daphnia from lakes with alewife, irrespective of the form of alewife predation, exhibited significantly larger eyes than Daphnia from lakes without alewife. This genetically based increase in eye size may enhance the ability of Daphnia to detect predators. Alternatively, such shifts in eye size may be an indirect response to Daphnia aggregating at the bottom of lakes. To test these mechanisms, we collected Daphnia as a function of depth and found that eye size differed in Daphnia found at the surface versus the bottom of the water column between anadromous alewife and no alewife lakes. However, we found no evidence of Daphnia aggregating at the bottom of lakes. Such results indicate that the evolution of a larger eye may be explained by a connection between eyes and enhanced survival. We discuss the cause of the lack of concordance in eye size variation between our phenotypic and genetic specimens and the ultimate drivers of eye size.

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

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.

Increased juvenile predation is not associated with evolved differences in adult brain size in Trinidadian killifish (Rivulus hartii).

Vertebrates exhibit extensive variation in brain size. The long-standing assumption is that this variation is driven by ecologically mediated selection. Recent work has shown that an increase in predator-induced mortality is associated with evolved increases and decreases in brain size. Thus, the manner in which predators induce shifts in brain size remains unclear. Increased predation early in life is a key driver of many adult traits, including life-history and behavioral traits. Such results foreshadow a connection between age-specific mortality and selection on adult brain size. Trinidadian killifish, Rivulus hartii, are found in sites with and without guppies, Poecilia reticulata. The densities of Rivulus drop dramatically in sites with guppies because guppies prey upon juvenile Rivulus. Previous work has shown that guppy predation is associated with the evolution of adult life-history traits in Rivulus. In this study, we compared second-generation laboratory-born Rivulus from sites with and without guppies for differences in brain size and associated trade-offs between brain size and other components of fitness. Despite the large amount of existing research on the importance of early-life events on the evolution of adult traits, and the role of predation on both behavior and brain size, we did not find an association between the presence of guppies and evolutionary shifts in Rivulus brain size. Such results argue that increased rates of juvenile mortality may not alter selection on adult brain size.

Predator-driven brain size evolution in natural populations of Trinidadian killifish (Rivulus hartii).

Vertebrates exhibit extensive variation in relative brain size. It has long been assumed that this variation is the product of ecologically driven natural selection. Yet, despite more than 100 years of research, the ecological conditions that select for changes in brain size are unclear. Recent laboratory selection experiments showed that selection for larger brains is associated with increased survival in risky environments. Such results lead to the prediction that increased predation should favour increased brain size. Work on natural populations, however, foreshadows the opposite trajectory of evolution; increased predation favours increased boldness, slower learning, and may thereby select for a smaller brain. We tested the influence of predator-induced mortality on brain size evolution by quantifying brain size variation in a Trinidadian killifish, Rivulus hartii, from communities that differ in predation intensity. We observed strong genetic differences in male (but not female) brain size between fish communities; second generation laboratory-reared males from sites with predators exhibited smaller brains than Rivulus from sites in which they are the only fish present. Such trends oppose the results of recent laboratory selection experiments and are not explained by trade-offs with other components of fitness. Our results suggest that increased male brain size is favoured in less risky environments because of the fitness benefits associated with faster rates of learning and problem-solving behaviour.