Abstract

Recently diverged taxa often show discordance in genetic divergence among genomic loci, where some loci show strong divergence and others show none at all. Genetic studies alone cannot distinguish among the possible mechanisms but experimental studies on other aspects of divergence may provide guidance in the inference of causes of observed discordances. In this study, we used no-choice mating trials to test for the presence of reproductive isolation between host races of the leaf-mining fly, Phytomyza glabricola on its two holly host species, Ilex coriacea and I. glabra. These trials inform our effort to determine the cause of significant differences in the degree of divergence of nuclear and mitochondrial loci of flies collected from the two host plants. We present evidence of reproductive isolation between host races in a controlled greenhouse setting: significantly more mate pairs consisting of flies from the same host plant species produced offspring than inter-host mate pairs, which produced no offspring. We also tested whether the presence of the natal or non-natal host plant affects reproductive success. Flies collected from I. coriacea were more likely to produce offspring when in the presence of the natal host, whereas the presence or absence of either the natal or non-natal host had no effect on flies collected from I. glabra. The results indicate discordant patterns of nuclear and mitochondrial divergence among host races of P. glabricola are likely due to incomplete lineage sorting, and the host races may be well on their way to becoming biological species.

Highlights

  • The evolution of new species results in genetic divergence among evolving lineages

  • The degree of genetic divergence among loci within the genome will vary depending on the differing effects of evolutionary mechanisms such as purifying selection (e.g., maintenance of housekeeping genes with reduced divergence [1] and divergent selection across an organism’s genome(s)

  • Trials were considered successful if the flies mated, the female oviposited eggs, and the offspring successfully emerged as adults. *Offspring emerged from I. coriacea in two of the trials and from I. glabra in three of the trials. doi:10.1371/journal.pone.0073976.t001

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Summary

Introduction

The evolution of new species results in genetic divergence among evolving lineages. The degree of genetic divergence among loci within the genome will vary depending on the differing effects of evolutionary mechanisms such as purifying selection (e.g., maintenance of housekeeping genes with reduced divergence [1] and divergent selection (e.g., genes involved in reproductive isolation with increased divergence [2,3,4]) across an organism’s genome(s). Neutral regions are expected to accumulate differences primarily via the relatively slow mechanisms of mutation and genetic drift, resulting in much slower sorting of differences into alternative lineages [5,6]. Neutral loci will be more-affected by introgression among lineages, resulting in discordance among different areas of the genome, between nuclear and organellar DNA (e.g., [7,8]). When there is discordance in the degree of divergence among different areas of the genome it can be difficult to distinguish introgression and episodic selection from incomplete lineage sorting as causes, when relying on genetic data alone. When complete reproductive isolation exists between genetically divergent populations, introgression is unlikely and explanations for discordance between markers swing towards incomplete lineage sorting [8], and the populations may be biological species [9]. If currently diverged populations mate and produce offspring, discordance among genomic regions may be due to introgression of alleles (e.g. [7,8])

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