Evolution of bower building in Lake Malawi cichlid fish: phylogeny, morphology, and behavior

Ryan A York,Russell D Fernald,Chinar Patil,C Darrin Hulsey,J Todd Streelman

doi:10.3389/fevo.2015.00018

Abstract

Despite considerable research, we still know little about the proximate and ultimate causes behind behavioral evolution. This is partly because understanding the forces acting on behavioral phenotypes requires the study of species-rich clades with extensive variation in behavioral traits, of which we have few current examples. In this paper, we introduce the bower-building cichlids of the Lake Malawi adaptive radiation, a lineage with over 100 species, each possessing a distinct male extended phenotype used to signal reproductive fitness. Extended phenotypes are useful units of analysis for the study of behavior since they are static structures that can be precisely measured within populations. To this end we recognize two core types of bowers - mounds (“castles”) and depressions (“pits”). We employ an established framework for the study of adaptive radiations to ask how traits related to other stages of radiations, macrohabitat and feeding morphology, are associated with the evolution of pit and castle phenotypes. We demonstrate that pits and castles are evolutionarily labile traits and have been derived numerous times in multiple Malawi genera. Using public ecological and phenotypic data sets we find significant and correlated differences in macrohabitat (depth), sensory ability (opsin expression), and feeding style (jaw morphology and biomechanics) between pit-digging and castle-building species. Phylogeny-corrected comparisons also show significant differences in several measures of jaw morphology while indicating non-significant differences in depth. Finally, using laboratory observations we assay courtship behaviors in a pit-digging (Copadichromis virginalis) and a castle-building species (Mchenga conophoros). Together, these results show that traits at multiple biological levels act to regulate the evolution of a courtship behavior within natural populations.

Highlights

Understanding the evolution of social behavior requires integration across diverse disciplines and methods (Tinbergen, 1963; Robinson et al, 2008; O’Connell and Hofmann, 2011; Hofmann et al, 2014) to identify and understand the proximate and ultimate mechanisms responsible
Pairwise comparisons of pit/pit-castle and castle/pitcastle species do not reveal any significant differences. These results indicate that castle-building species tend to occur at shallower maximum depths with less variation in depth range than pit-digging species
Since single-cone opsins are sensitive to shorter wavelengths, we tested for differences in single and double cone sensitivities that might corroborate the differential expression of SWS2b

Summary

Introduction

Understanding the evolution of social behavior requires integration across diverse disciplines and methods (Tinbergen, 1963; Robinson et al, 2008; O’Connell and Hofmann, 2011; Hofmann et al, 2014) to identify and understand the proximate and ultimate mechanisms responsible. Given increased availability of data sets that include diverse species, several groups have used multidisciplinary methods to identify traits that regulate social behavior among several taxa (Goodson, 2005; Pollen et al, 2007; Lefebvre and Sol, 2008). We would like to analyze clades rich with species displaying high levels of diversity in brain anatomy, function, genetics, and social behavior, allowing multi-dimensional comparisons of traits. Such an approach requires use of appropriate modern molecular and neurobiological methods. Bower-building cichlid fish of Lake Malawi are an outstanding example of a clade of species appropriate for discovering the relationships amongst multiple variables that have shaped important differences in this diverse collection of species over evolutionary time.

Methods

Results

Discussion

Conclusion