Fast life-histories are associated with larger brain size in killifishes.

Will Sowersby,Simon Eckerström‐Liedholm,Alexander Kotrschal,Piotr Rowiński,Joacim Näslund,Alejandro Gonzalez‐Voyer,Björn Rogell

doi:10.1111/evo.14310

Abstract

The high energetic demands associated with the vertebrate brain are proposed to result in a trade-off between the pace of life-history and relative brain size. However, because both life-history and brain size also have a strong relationship with body size, any associations between the pace of life-history and relative brain size may be confounded by coevolution with body size. Studies on systems where contrasts in the pace of life-history occur without concordant contrasts in body size could therefore add to our understanding of the potential coevolution between relative brain size and life-history. Using one such system - 21 species of killifish - we employed a common garden design across two ontogenetic stages to investigate the association between relative brain size and the pace of life-history. Contrary to predictions, we found that relative brain size was larger in adult fast-living killifishes, compared to slow-living species. Although we found no differences in relative brain size between juvenile killifishes. Our results suggest that fast- and slow-living killifishes do not exhibit the predicted trade-off between brain size and life-history. Instead, fast and slow-living killifishes could differ in the ontogenetic timing of somatic versus neural growth or inhabit environments that differ considerably in cognitive demands.

Highlights

Variation in brain size across species is largely driven by the cognitive benefits and the energetic costs of developing and maintaining a large brain
As body size often displays higher evolutionary rates than brain size (Gonzalez-Voyer et al 2009b; Smaers et al 2012; see Tsuboi et al 2018) any condition that imposes selection on body size may result in correlated responses with the brain that are lower than would be expected from an evolutionary allometry perspective
The evolutionary brain-body size allometries among species were hypoallometric [fast-living species, adults – βslope: 0.461 (0.329, 0.563); slowliving species adults – βslope: 0.446 (0.327, 0.552); fast-living species, juveniles – βslope: 0.637 (0.426; 0.812); slow-living species, juveniles – βslope: 0.514 (0.297; 0.752)]

Summary

Introduction

Variation in brain size across species is largely driven by the cognitive benefits and the energetic costs of developing and maintaining a large brain (benefits: Lefebvre et al 1997, Lefebvre et al 2004; McDaniel 2005; Sol et al 2008; Maklakov et al 2011; Kotrschal et al 2013, Kotrschal et al 2015a, Kotrschal et al.2015b; MacLean et al 2014; Benson-Amram et al 2016; Heldstab et al 2016, and costs: Wang et al 2012; Kotrschal et al 2013; Gonzalez-Voyer et al 2016). Killifishes have undergone at least seven independent evolutionary transitions toward living in ephemeral habitats, where an ability to produce eggs capable of entering an extended embryonic diapause stage allows populations to persist during habitat desiccation (Furness et al 2015; Furness 2016, Gonzalez-Voyer et al in prep.) These annual killifishes have evolved several fast-paced life-history traits necessary for living in time-limited ephemeral habitats, including on average 1.3 times faster growth rate, shorter development periods, and seven times higher reproductive rate (EckerströmLiedholm et al 2017; Sowersby et al preprint). One hypothesized benefit of inhabiting these harsh and time-limited ephemeral environments is that they are considered to be relatively inaccessible to many aquatic predators (Werner and McPeek 1994; Fraser et al 1995) and attract fewer piscivorous birds, compared to more permanent habitats (Mamboleo et al 2012)

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Discussion

Conclusion