Abstract

Contrasting phenotypes arise from similar genomes through a combination of losses, gains, co-option and modifications of inherited genomic material. Understanding the molecular basis of this phenotypic diversity is a fundamental challenge in modern evolutionary biology. Comparisons of the genes and their expression patterns underlying traits in closely related species offer an unrivaled opportunity to evaluate the extent to which genomic material is reorganized to produce novel traits. Advances in molecular methods now allow us to dissect the molecular machinery underlying phenotypic diversity in almost any organism, from single-celled entities to the most complex vertebrates. Here we discuss how comparisons of social parasites and their free-living hosts may provide unique insights into the molecular basis of phenotypic evolution. Social parasites evolve from a eusocial ancestor and are specialized to exploit the socially acquired resources of their closely-related eusocial host. Molecular comparisons of such species pairs can reveal how genomic material is re-organized in the loss of ancestral traits (i.e., of free-living traits in the parasites) and the gain of new ones (i.e., specialist traits required for a parasitic lifestyle). We define hypotheses on the molecular basis of phenotypes in the evolution of social parasitism and discuss their wider application in our understanding of the molecular basis of phenotypic diversity within the theoretical framework of phenotypic plasticity and shifting reaction norms. Currently there are no data available to test these hypotheses, and so we also provide some proof of concept data using the paper wasp social parasite/host system (Polistes sulcifer—Polistes dominula). This conceptual framework and first empirical data provide a spring-board for directing future genomic analyses on exploiting social parasites as a route to understanding the evolution of phenotypic specialization.

Highlights

  • THE MOLECULAR BASIS OF PHENOTYPIC DIVERSITYEvolution plays with inherited traits to produce altered phenotypes which may be better adapted to fill a niche different to that of their ancestors

  • Genomic methods in modern evolutionary biology allow us to dissect the molecular basis of such phenotypic diversity across a range of organisms, from genes to phenotypes (Tautz et al, 2010)

  • The scant data available to date suggest that the social parasite phenotype is distinct from their eusocial ancestor counter-part

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Summary

Introduction

THE MOLECULAR BASIS OF PHENOTYPIC DIVERSITYEvolution plays with inherited traits to produce altered phenotypes which may be better adapted to fill a niche different to that of their ancestors. Comparisons of the molecular bases of closely related host and social parasite traits will provide new insights into phenotypic evolution. We identify the key traits of hymenopteran social parasites of eusocial insects that make them useful models for understanding phenotypic evolution at the molecular level.

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