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

Abstract

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.

Keywords: boldness; brain size; killifish; life-history evolution; predation.

Figure 1.

Variation in brain size between predator communities. (a) Male absolute brain size, (b) female absolute brain size, (c) male length versus brain size, (d) female length versus brain size, (e) male relative brain size, and (f) female relative brain size. Panels (a,b) and (e,f): grey squares indicate population means, filled circles indicate replicate river means. Panels (c,d): filled circles (solid regression line)—high predation fish, open circles (dashed regression line)—Rivulus-only fish. The regression lines between fish size and brain size are based upon the raw data. We observed significant (p < 0.05) interactions between sex and predation for absolute and relative brain size. Small differences were observed between Rivulus from high predation (HP) and Rivulus-only (RO) sites for females but such differences were much larger in males. The data points for male and female relative brain size reflect the estimated marginal means at the mean of the covariate. Error = ±1 s.e.

Figure 2.

Variation in gut size between predator communities. (a) Male relative gut size, (b) female relative gut size, (c) male length versus gut size, and (d) female length versus gut size. Panels (a,b) and (e,f): grey squares indicate population means, filled circles indicate replicate river means. Panels (c,d): filled circles (solid regression line)—high predation fish, open circles (dashed regression line)—Rivulus-only fish. The regression lines between fish size and brain size are based upon the raw data. The predation × sex was significant (p < 0.05). Males from high predation sites exhibited a smaller gut size than Rivulus from Rivulus-only sites but such trends were opposite in females. The data points for male and female relative gut size reflect the estimated marginal means at the mean of the covariate. Error = ±1 s.e.

Figure 3.

Correlations between male brain size, gut size, and age at maturation. (a) Brain size versus age at maturation for high predation males, (b) brain size versus age at maturation for Rivulus-only males, (c) brain size versus gut size for high predation males, and (d) brain size versus gut size for Rivulus-only males. Open circles (solid regression line), Arima River; filled circles (dashed regression line), Guanapo River. All correlations were not significant (p > 0.05).