Abstract

Adaptive radiation occurs when the members of a single lineage evolve different adaptive forms in response to selection imposed by competitors or predators. Iconic examples include Darwin's finches, Caribbean anoles, and Hawaiian silverswords, all of which live on islands. Although adaptive radiation is thought to be an important generator of biodiversity, most studies concern groups that have already diversified. Here, we take the opposite approach. We experimentally triggered diversification in the descendants of a single population of host‐specific parasites confined to different host “islands.” We show rapid adaptive divergence of experimentally evolving feather lice in response to preening, which is a bird's main defense against ectoparasites. We demonstrate that host defense exerts strong phenotypic selection for crypsis in lice transferred to different colored rock pigeons (Columba livia). During four years of experimental evolution (∼60 generations), the lice evolved heritable differences in color. Strikingly, the observed color differences spanned the range of phenotypes found among congeneric lice adapted to other species of birds. To our knowledge, this is the first real‐time demonstration that microevolution is fast enough to simulate millions of years of macroevolutionary change. Our results further indicate that host‐mediated selection triggers rapid divergence in the adaptive radiation of parasites, which are among the most diverse organisms on Earth.

Highlights

  • Adaptive radiation is a major source of organismal diversity [1,2,3,4,5]

  • One of the challenges of experimental work with host-specific parasites is that, by definition, they are difficult to culture in sufficient numbers on novel host species

  • We circumvented this problem by working with rock pigeons (Columba livia), a single host species that harbors extensive intraspecific diversity in color as a result of artificial selection [26]

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Summary

Introduction

Adaptive radiation is a major source of organismal diversity [1,2,3,4,5]. Ironically, the role of this process in parasite diversification remains unclear, despite the fact that parasites are among the most diverse organisms on Earth [6,7,8,9,10]. There was no significant difference in the number of cryptic and conspicuous lice on pigeons with impaired preening (Fig. 2G). Because feather lice are permanent parasites that pass their entire life cycle on the body of the host, they can be evolved experimentally under natural conditions on captive birds.

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