American Society of Naturalists

Christopher G. Mull, Kara E. Yopak, and Nicholas K. Dulvy (June 2020)

Shark and ray brain organization varies along a gradient reflecting size, maternal investment, and ecological lifestyle

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While the drivers of brain size evolution have received lots of attention over the past several decades, there has been considerably less examination of the correlates of brain organization evolution – the relative size of the five major regions that comprise vertebrate brains. Because the relative size of a brain region potentially reflects its importance, most studies have looked for ecological or behavioral correlates of brain organization while ignoring the effects of life history (the rate of growth, maturation, and form of reproduction).

Chondrichthyans (sharks, rays, and chimaeras) are an often overlooked yet remarkably diverse group. Their lineage represents the oldest jawed vertebrates and comprises more than 1,200 species that inhabit every aquatic habitat on earth and exhibit most described reproductive modes, from egg-laying to placental live-bearing. They also mark the evolutionary origin of the vertebrate brain archetype characterized by five distinct regions, including the first true cerebellum. Because of their diversity, chondrichthyans are an excellent group for tackling fundamental questions about brain evolution.

A new study led by Christopher Mull with colleagues from Simon Fraser University and the University of North Carolina Wilmington tackled these questions by collecting and examining the brains of 100 species of chondrichthyans spanning every major order, ecological lifestyle, and reproductive mode. They found that brain organization varies across a series of axes rather than distinctly with ecology. Deep-water species tended to have low levels of maternal investment, with small brains predominantly comprised of medulla – important for non-visual sensory integration. Species with higher levels of maternal investment inhabiting shallow complex habitats, such as reefs, have relatively large brains comprised predominantly of telencephalon – important for higher cognitive functions such as spatial learning. For the first time, the researchers demonstrate that both ecological lifestyle and maternal investment are independently associated with brain organization. These findings highlight the need for a more holistic approach to understanding the evolution of brain size and organization across vertebrates.

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Abstract

Across vertebrates increased maternal investment (via increased pre- and postnatal provisioning) is associated with larger relative brain size, yet it remains unclear how brain organization is shaped by life history and ecology. Here, we tested whether maternal investment and ecological lifestyle are related to variation in brain size and organization across 100 chondrichthyans. We hypothesized that brain size and organization would vary with level of maternal investment and habitat depth and complexity. We found that chondrichthyan brain organization varies along four main axes, according to: (1) absolute brain size, (2) relative diencephalon and mesencephalon size, (3) relative telencephalon and medulla size, and (4) relative cerebellum size. Increased maternal investment is associated with larger relative brain size, while ecological lifestyle is informative for variation between relative telencephalon and medulla size, and relative cerebellum size after accounting for the independent effects of reproductive mode. Deep-water chondrichthyans generally provide low levels of yolk-only (lecithotrophic) maternal investment and have relatively small brains, predominantly comprised of medulla (a major portion of the hindbrain). Whereas, matrotrophic chondrichthyans – which provide maternal provisioning beyond the initial yolk-sac – found in coastal, reef, or shallow oceanic habitats have large relative brain sizes, predominantly comprised of telencephalon (a major portion of the forebrain). We demonstrated, for the first time, that both ecological lifestyle and maternal investment are independently associated with brain organization in a lineage with diverse life history strategies and reproductive modes.