Brain size affects female but not male survival under predation threat

Abstract

There is remarkable diversity in brain size among vertebrates, but surprisingly little is known about how ecological species interactions impact the evolution of brain size. Using guppies, artificially selected for large and small brains, we determined how brain size affects survival under predation threat in a naturalistic environment. We cohoused mixed groups of small- and large-brained individuals in six semi-natural streams with their natural predator, the pike cichlid, and monitored survival in weekly censuses over 5 months. We found that large-brained females had 13.5% higher survival compared to small-brained females, whereas the brain size had no discernible effect on male survival. We suggest that large-brained females have a cognitive advantage that allows them to better evade predation, whereas large-brained males are more colourful, which may counteract any potential benefits of brain size. Our study provides the first experimental evidence that trophic interactions can affect the evolution of brain size.

Predation pressure shapes brain anatomy in the wild

“…From the prey side, the cognitive advantage of a larger brain can lead to increased survival. This was recently shown in guppies (Poecilia reticulata) that were artificially selected for large and small brain size where large-brained females survived better under predation in a seminatural setting (Kotrschal et al 2015a). However, Walsh et al (2016) found that in two areas where killifish (Rivulus hartii) co-occur with predatory fish species, males tended to develop smaller brains than in two adjacent areas where the killifish was not under threat from fish predators.…”

“…We do this by relating data on predator community composition to brain anatomy of guppies from 16 wild populations that are closely matched in stream characteristics (Deacon et al 2015). Because a larger brain confers a cognitive advantage and so improves predator-related performance (Kotrschal et al 2015a;van der Bijl et al 2015), we predict that increased predation pressure selects for larger brains. This would result in a positive association across populations between brain size and the abundance of individual predators.…”

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

“…Such trends largely parallel those observed in Rivulus between sites with and without large predators (for males only) (Walsh et al., 2016) although the brain size differences in sticklebacks were not maintained in common garden‐reared fish (Gonda et al., 2011). Conversely, work on captive populations of guppies showed that selection for a larger brain is associated with enhanced survival in risky habitats (Kotrschal et al., 2015a). This growing body of work clearly provides a connection between predators and brain size, although the contradictory nature of these results currently limits our understanding of the manner in which predatory selection acts on brain size.…”

“…There are clear fitness benefits associated with a larger brain as brain size is positively correlated with increased intelligence, cognition, learning capability, population persistence, and decreased susceptibility to predation (Sol & Lefebvre, 2000; Tebbich & Bshary, 2004; Shultz & Dunbar, 2006a; Sol, Szekely, Liker, & Lefebvre, 2007; Sol, Bacher, Reader, & Lefebvre, 2008; Overington, Morand‐Ferron, Boogert, & Lefebvre, 2009; Barrickman, Bastian, Isler, & van Schaik, 2008; Amiel, Tingley, & Shine, 2011; Reader, Hager, & Laland, 2011; Kotrschal et al., 2013b; MacLean et al., 2014; Kotrschal et al., 2015a; Kotrschal, Corral‐Lopez, Amcoff, & Kolm, 2015b; Benson‐Amram, Dantzer, Stricker, Swanson, & Holekamp, 2016; but also see Drake, 2007). Key hypotheses, such as the expensive tissue hypothesis (i.e., expensive metabolic cost of brain tissue) (Aiello & Wheeler, 1995; Isler & van Schaik, 2009) and energy trade‐off hypothesis (increased encephalization leads to trade‐offs with other functions) (Isler & van Schaik, 2006a,b, 2009; Navarrete, van Schaik, & Isler, 2011; Tsuboi et al., 2015), recognize that brain tissue is costly and that fitness trade‐offs likely underlie increased encephalization (Aiello & Wheeler, 1995).…”

“…Male Rivulus with larger brains are potentially favored in safer environments due to the fitness benefits that may result from better problem‐solving behavior and increased cognition (Walsh et al., 2016). The current literature clearly illustrates a connection between predation regime and brain size evolution, but given the inconsistent nature of the results from this growing body of work (van der Bijl et al., 2015; Burns & Rodd, 2008; Gonda, Herczeg, & Merila, 2009a,b, 2011; Kotrschal et al., 2015a; Shultz & Dunbar, 2006b; Walsh et al., 2016), the generality of such conclusions requires further testing.…”