Evolution of vertebrate brain size: an experimental approach

Why is the human brain so different from that of any other animal species? What are the evolutionary events in vertebrates that have led to the human brain? These questions have fascinated evolutionary biologists for centuries and continue to be key issues in modern evolutionary biology. A massive research effort in this area over the last decade has produced considerable evidence about the selective pressures that have shaped the evolution of the enormous variation in brain size among vertebrates. Comparative studies relating both within- and between species variation in brain size to a variety of ecological and behavioural traits have uncovered some of the evolutionary pathways by which contemporary species have adapted to their physical and social environment. But while comparative studies are an essential first step in understanding the evolutionary events leading towards the human brain, these studies lack the conclusive evidence only acquired by proper experimental testing. The project outlined here aims at filling this gap by experimentally testing the key issues in the study of brain size evolution. Specifically the project will make use of the small- and large-brained guppy lines (Poecilia reticulata; brain weight selected lines - BWS lines), that I recently developed in Niclas Kolm`s group at the EBC at Uppsala University to investigate the potential costs and benefits of having small or large brains. I first want to concentrate on the behavioural consequences of large and small brains and compare cognitive ability between the lines. With this unique system I then aim to investigate the consequences of differential investment into brain development. Since the brain is among the most costly organs to build and maintain, a selection on relative brain size will inevitably reveal trade-offs with other body parts. I will examine differences in secondary sexual characters in males (costly ornaments like carotenoid spots and fin- and gonopodium size and behaviours like competitiveness and courtship vigour) and life-history traits in females (fecundity, offspring size, time to maturation) and directly linked to these questions I will test courtship success by genotyping sperm donated in females and offspring from mixed groups in large semi-natural tanks. Further trade-offs suggested by theory and comparative studies, which I am eager to test, include longevity, gut size and aspects of physiology such as metabolic rate. But I will also investigate how brain morphology changes in response to a strong selection on brain size and therefore examine whether some brain structures respond more to selection and whether it is neuron size or neuron number that changes to produce brain size differences. Finally I will use quantitative genetic tools to explore the variance and covariance between brain size, body size and life history in the existing pedigree of approximately 2000 breeder individuals spanning five generations. To tackle these questions I will collaborate with numerous leading scientists, supervise three masters students and hope to transfer the acquired know-how to Austria when moving back to Vienna.

Why is the human brain so different from that of any other animal species? What are the evolutionary events in vertebrates that have led to the human brain? These questions have fascinated evolutionary biologists for centuries and continue to be key issues in modern evolutionary biology. A massive research effort in this area over the last decade has produced considerable evidence about the selective pressures that have shaped the evolution of the enormous variation in brain size among vertebrates. Comparative studies relating both within- and between species variation in brain size to a variety of ecological and behavioural traits have uncovered some of the evolutionary pathways by which contemporary species have adapted to their physical and social environment. However, comparative analyses can never establish causality only experiments can do so. With the this project we started to fill this void. We used the large- and small-brained guppies (Poecilia reticulata), which I have bred previous to my Schrödinger fellowship in Niclas Kolms group at the University of Uppsala, Sweden, to investigate the costs and benefits of evolving a large vs. a small brain. We could show that large-brained individuals show a better learning performance than small-brained ones. This is the first experimental evidence for a cognitive benefit of a relatively larger brain. Since the brain is among the most energetically expensive organs, selecting on its size will inevitably lead to a trade-off with other costly organs. Indeed we could show a decreased reproductive output and smaller guts in large-brained fish. Because ornaments of mate choice are also energetically costly, we expected that large-brained males exhibit smaller or less prominent sexual ornaments (such as less colourful patterns). The opposite was the case, because large-brained males showed not only more colours, but also longer tail fins and longer gonopodiums (the male intermittent organ). This surprising result helped us reconsidering the nature of the link between brain size evolution and sexually selected ornaments, namely that selection on body condition may favour both large brains and more attractive sexual ornaments. Further projects included how brain size impacts animal personalities, their physiology and their mat choice. The to date most sensational finding of our project is the discovery of a brain size gene. In collaboration with the University College London and Helsinki University we used cutting edge molecular genetic tools to identify a single gene that is expressed differently in large- and small-brained animals. We manipulated the expression of this gene in zebra fish and indeed could so change the brain size of those fish. Currently there are numerous follow-up experiments underway; those include a study on the survival advantage a relatively large brain confers under naturalistic conditions.