Field Studies Reveal Strong Postmating Isolation between Ecologically Divergent Butterfly Populations

Carolyn S. McBride,Michael C. Singer

doi:10.1371/journal.pbio.1000529

Carolyn S. McBride, Michael C. Singer

Open Access

https://doi.org/10.1371/journal.pbio.1000529

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Abstract

Author SummaryWhen two populations adapt to different ecological environments, they may become reproductively incompatible with each other and eventually form distinct species. One form of incompatibility thought to contribute to this process occurs when hybrids between diverging populations are ecologically maladapted. They suffer reduced survival and reproduction because they possess intermediate traits that are ill-suited to both parental environments. Although this phenomenon is potentially important at the early stages of speciation, it is difficult to study in the field and is often invisible in the laboratory—leaving us with few empirical examples. We use a series of behavioral assays and manipulative field experiments to examine hybrids between populations of a butterfly that have adapted to use distinct host plants. We show that the hybrids are perfectly healthy in the laboratory. However, when taken into the field, they interact with their host plants in intermediate and anomalous ways that lower the growth and survival of both themselves and their offspring. Our findings confirm that ecological selection against hybrids has great potential to block gene flow at the early stages of adaptive divergence.

Highlights

The idea that ecological divergence can drive speciation has been discussed, studied, and widely accepted since the time of Darwin [1,2,3,4,5,6,7,8,9]
One form of incompatibility thought to contribute to this process occurs when hybrids between diverging populations are ecologically maladapted. They suffer reduced survival and reproduction because they possess intermediate traits that are ill-suited to both parental environments. This phenomenon is potentially important at the early stages of speciation, it is difficult to study in the field and is often invisible in the laboratory— leaving us with few empirical examples
We use a series of behavioral assays and manipulative field experiments to examine hybrids between populations of a butterfly that have adapted to use distinct host plants

Summary

Introduction

The idea that ecological divergence can drive speciation has been discussed, studied, and widely accepted since the time of Darwin [1,2,3,4,5,6,7,8,9]. Such adaptation will reduce gene flow between the populations if hybrids have intermediate phenotypes that fare poorly in both parental habitats—in essence, if hybrids fall in an adaptive valley between the fitness peaks associated with the niches of their parents This phenomenon is called extrinsic postzygotic isolation (EPI) because it obstructs gene flow after hybrid zygotes have formed ( postzygotic) and arises from an interaction between hybrids and their environment rather than from inherent developmental defects ( extrinsic). EPI has the potential to act in any system involving ecological divergence, regardless of its biological particulars This sets it apart from several forms of prezygotic isolation, which can only contribute to speciation when the alternative niches are directly linked to mate choice (e.g., habitat isolation, temporal isolation, pollinator isolation, and sexual isolation based on ecological traits that double as mating cues [6,8])

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