Abstract

BackgroundThe formation of reproductive barriers in diverging lineages is a prerequisite to complete speciation according to the biological species concept. In parasites with complex life cycles, speciation may be driven by adaptation to different intermediate hosts, yet diverging lineages can still share the same definitive host where reproduction takes place. In these cases, prezygotic isolation mechanisms should evolve very early and be particularly strong, preventing costly unfavourable matings.In this study, we investigated the importance of prezygotic barriers to reproduction in two cestode species that diverged 20–25mya and show an extraordinary degree of specificity to different intermediate hosts. Both species share the same definitive hosts and hybridize in the laboratory. Yet, natural hybrids have so far not been detected.MethodsWe used a combination of different experiments to investigate the role of prezygotic barriers to reproduction in the speciation of these parasites. First, we investigated whether hybridization is possible under natural conditions by exposing lab-reared herring gulls (Larus argentatus, the definitive hosts) to both parasites of either sympatric or allopatric combinations. In a second experiment, we tested whether the parasites prefer conspecifics over parasites from a different species in dichotomous mate choice trials.ResultsOur results show that the two species hybridize under natural conditions with parasites originating either from sympatric or allopatric populations producing hybrid offspring. Surprisingly, the mate choice experiment indicated that both parasite species prefer mates of the different species to conspecifics.ConclusionsNeither fundamental constraints against hybridization in a natural host nor assortative mate choice sufficiently explain the persistent segregation of the two tapeworm species in nature. Hence, postzygotic ecological selection against hybrids is presumably the more important driving force limiting gene flow between the two parasite sister species.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0799-5) contains supplementary material, which is available to authorized users.

Highlights

  • The formation of reproductive barriers in diverging lineages is a prerequisite to complete speciation according to the biological species concept

  • Both parasites are highly specific on this level of the life cycle: S. solidus can only infect threespined sticklebacks (Gasterosteus aculeatus), while S. pungitii is only infective to nine-spined sticklebacks (Pungitius pungitius)

  • The experiment clearly showed that the hybridization between S. solidus and S. pungitii is not a laboratory artefact and that both worm species shared the same microhabitat within the gut of the herring gull for a time span long enough to enable a successful cross-species mating

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Summary

Introduction

The formation of reproductive barriers in diverging lineages is a prerequisite to complete speciation according to the biological species concept. In parasites with complex life cycles, speciation may be driven by adaptation to different intermediate hosts, yet diverging lineages can still share the same definitive host where reproduction takes place. In these cases, prezygotic isolation mechanisms should evolve very early and be strong, preventing costly unfavourable matings. We investigated the importance of prezygotic barriers to reproduction in two cestode species that diverged 20–25mya and show an extraordinary degree of specificity to different intermediate hosts Both species share the same definitive hosts and hybridize in the laboratory. Selection against hybrids may lead to reinforcement, thereby increasing reproductive isolation of the parental species [7]

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