Abstract
Plant-herbivore interactions promote the generation and maintenance of both plant and herbivore biodiversity. The antagonistic interactions between plants and herbivores lead to host race formation: the evolution of herbivore types specializing on different plant species, with restricted gene flow between them. Understanding how ecological specialization promotes host race formation usually depends on artificial approaches, using laboratory experiments on populations associated with agricultural crops. However, evidence on how host races are formed and maintained in a natural setting remains scarce. Here, we take a multidisciplinary approach to understand whether populations of the generalist spider mite Tetranychus urticae form host races in nature. We demonstrate that a host race co-occurs among generalist conspecifics in the dune ecosystem of The Netherlands. Extensive field sampling and genotyping of individuals over three consecutive years showed a clear pattern of host associations. Genome-wide differences between the host race and generalist conspecifics were found using a dense set of SNPs on field-derived iso-female lines and previously sequenced genomes of T. urticae. Hybridization between lines of the host race and sympatric generalist lines is restricted by post-zygotic breakdown, and selection negatively impacts the survival of generalists on the native host of the host race. Our description of a host race among conspecifics with a larger diet breadth shows how ecological and reproductive isolation aid in maintaining intra-specific variation in sympatry, despite the opportunity for homogenization through gene flow. Our findings highlight the importance of explicitly considering the spatial and temporal scale on which plant-herbivore interactions occur in order to identify herbivore populations associated with different plant species in nature. This system can be used to study the underlying genetic architecture and mechanisms that facilitate the use of a large range of host plant taxa by extreme generalist herbivores. In addition, it offers the chance to investigate the prevalence and mechanisms of ecological specialization in nature.
Highlights
Plant-herbivore interactions promote the generation and maintenance of both plant and herbivore biodiversity
We present clear evidence for the occurrence of a specialist T. urticae host race, which is isolated from conspecifics by a post-zygotic barrier to gene flow, and that is genetically differentiated from sympatric generalist conspecifics that co-occur with the host race at small spatial scales
We present evidence of intraspecific population structure related to host use and incomplete reproductive isolation in the generalist herbivore T. urticae
Summary
Plant-herbivore interactions promote the generation and maintenance of both plant and herbivore biodiversity. Our findings highlight the importance of explicitly considering the spatial and temporal scale on which plant-herbivore interactions occur in order to identify herbivore populations associated with different plant species in nature This system can be used to study the underlying genetic architecture and mechanisms that facilitate the use of a large range of host plant taxa by extreme generalist herbivores. Herbivores with large geographic ranges may encounter a myriad of plant taxa, some more heavily defended against herbivory than others This results in a mosaic of locally available hosts, in which herbivore population structure can arise due to spatially and temporally varying selection, resulting in local adaptation and extinction events[19,20]. The role of host adaptation in promoting population structure and reproductive isolation in T. urticae in nature is not clear, as it is uncertain whether it is a complex of host races or whether its breadth in host range reflects variation in host preference[33,34,35] or plasticity in its molecular toolkit[36,37,38,39,40,41,42,43,44,45,46,47]
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