Adaptive divergence and post-zygotic barriers to gene flow between sympatric populations of a herbivorous mite

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.

Incipient sympatric speciation via host race formation in Phengaris arion (Lepidoptera: Lycaenidae)

The plausibility of sympatric speciation is still debated despite increasing evidence, such as host races in insects. This speciation process may be occurring in the case of the two phenological forms of the obligatorily myrmecophilous Phengaris arion. The main goal of our research was to study the nature and causes of difference between these forms focusing primarily on the incipient speciation via host races. Molecular analyses based on highly variable microsatellites together with Wolbachia screening, male genitalia morphometrics and host ant studies were carried out on four syntopic sample pairs. Our results show that the two phenological forms of P. arion may meet the criteria for host plant races. They coexist in sympatry in certain parts of the species range which is allowed by the adaptation to the distinct phenology of the host plants. Negative selection acts against the intermediate individuals which are on the wing in the inappropriate time frame. Thus, disruptive selection affects and produces bimodal distributions of phenotypes. However, the phenology of food plants is not entirely distinct and fluctuates year by year. Therefore, the two forms can exchange genes occasionally depending on the length of the time slot when they can meet with each other. Consequently, the reproductive isolation could not be completed and the existence of the two arion forms may represent only an incipient stage of sympatric speciation. It is also clear that Wolbachia is likely not a driver of sympatric speciation in this case.