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

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.

Abundant trans-driven variation in detoxification gene expression in the extreme generalist herbivore Tetranychus urticae

“…Among the five strains, variant prediction revealed 1.19 million high-quality variants (SNPs and small indels), consistent with prior studies that have revealed substantial variation among T. urticae strains [51][52][53][54]. Further, more than 98% of SNP sites were fixed in each of the five strains, confirming earlier reports that ~7 generations of inbreeding in this haplodiploid species results in isogenic (or nearly isogenic) strains [52].…”

“…urticae strains [51][52][53][54]. Further, more than 98% of SNP sites were fixed in each of the five strains, confirming earlier reports that ~7 generations of inbreeding in this haplodiploid species results in isogenic (or nearly isogenic) strains [52].…”

“…The PCA was performed on the GDS file converted from the VCF using gdsfmt (version 0.18.1) [102,103] with the option "method=copy.num.of.ref" (which includes all SNPs). Further, we confirmed that the five strains were in fact isogenic, as expected for inbred strains, by determining the fraction of variable SNPs in each parental strain that were fixed (i.e., homozygous; see Results); to do this, we used the approach of Villacis-Perez et al [54].…”

“…Further, the strains we used captured variation in host plant use representative of that observed in earlier studies with this species [51,54,75].…”

“…Previously, variation in the performance of T. urticae strains on different host plants raised the possibility of host race formation within this species. Despite a striking recent example [54, 77], comparatively little evidence exists for wide-spread host-race formation in T. urticae , where host plant adaptation can occur in as few as five generations [33], and seasonal or yearly movement of T. urticae populations among host plants is likely common. Our finding that trans regulation is most often observed in T. urticae may reflect this, and contrasts to findings in species like the monkeyflower Erythranthe guttata (formerly Mimulus guttatus ) and the threespine stickleback fish ( Gasterosteus aculeatus ) for which a predominance of intraspecific cis variation has been associated with evolutionary divergent subpopulations (i.e., costal versus inland populations of monkeyflower, and marine versus freshwater populations in the stickleback) [19, 78].…”