The potential of a population genomics approach to analyse geographic mosaics of plant--insect coevolution

Abstract

A central issue in the evolutionary ecology of species interactions is coevolution, which involves the reciprocal selection between individuals of interacting species. Understanding the importance of coevolution in shaping species interactions requires the consideration of spatial variation in their strength. This is exactly what the, recently developed, geographic mosaic theory of coevolution addresses. Another major development in the study of population ecology is the introduction of the population genomics approach in this field of research. This approach addresses spatial processes through molecular methods. It is of particular interest that population genomics is especially applicable to natural populations of non-model species. We describe how population genomics can be used in the context of the geographic mosaic of coevolution, specifically to identify coevolutionary hot-spots, and to attribute genetic variation found at specific loci to processes of selection versus trait remixing. The proposed integration of the population genomics approach with the conceptual framework of the geographic mosaic of coevolution is illustrated with a few selected, particularly demonstrative, examples from the realm of insect-plant interactions.

Comparative genetics of invasive populations of walnut aphid, Chromaphis juglandicola, and its introduced parasitoid, Trioxys pallidus, in California

“…Using the approach of Vermeer et al. (), results suggested that Escalon, Newark, and Upper Lake potentially represent coevolutionary hot spots, while Arbuckle, Linden, and Yuba City potentially represent coevolutionary cold spots. However, Bayesian simulations using BayeScan indicated that none of the potential outliers for either species showed significant ( p < .05) signatures of selection.…”

“…However, as Vermeer et al. () outline, for this approach to provide more than preliminary evidence for the presence of a geographic mosaic of coevolution, genotype data from a large number of independent neutral loci (preferably single nucleotide polymorphisms [SNPs]) need be compared to phenotypic measurements from traits of interest, as has been done in other systems (e.g., Dupas, Dubuffet, Carton, & Poire, ; Jancek et al., ; Parchman, Benkman, Jenkins, & Buerkle, ; Parchman et al., ). Given that our current study includes genotype data only, and from a relatively small number of microsatellite loci, we are not yet able to determine whether the presence of outlier loci in both species is the result of reciprocal selection, or of random chance.…”

“…, Luikart et al ,. Stinchcombe & Hoekstra ; Deagle et al., ; Barker, Andonian, Swope, Luster, & Dlugosch, ) and coevolutionary processes (Parchman, Buerkle, Soria‐Carrasco, & Benkman, ; Vermeer, Dicke, & de Jong, ; Yoder, ). Through the examination of large numbers of neutral markers, population genomics can be used to separate locus‐specific effects that may be linked to genes under selection, from genomewide effects driven by genetic drift, migration, and inbreeding.…”

“…In this context, Vermeer et al. () suggest that while population genomics cannot be used to test for the existence of a geographic mosaic of coevolution per se, it can be a valuable approach for the detection of unusual levels of variation or “outliers” at specific loci that are potential indicators of hot spots of reciprocal selection, and for estimation of the extent of gene flow and inbreeding that are factors contributing to trait remixing.…”

“…One of the key difficulties in finding evidence for coevolution is the identification of the ecologically relevant traits or genes that are under reciprocal selection in antagonistic interactions. Recently, population genomics has been utilized to facilitate our understanding of evolutionary (Black et al 2001, Luikart et al 2003, Stinchcombe & Hoekstra 2008Deagle et al, 2011;Barker, Andonian, Swope, Luster, & Dlugosch, 2017) and coevolutionary processes (Parchman, Buerkle, Soria-Carrasco, & Benkman, 2016;Vermeer, Dicke, & de Jong, 2011;Yoder, 2016). Through the examination of large numbers of neutral markers, population genomics can be used to separate locus-specific effects that may be linked to genes under selection, from genomewide effects driven by genetic drift, migration, and inbreeding.…”