Variable genomic patterns of hybridization in two independent hybrid zones of damselflies

Abstract

Hybrid zones with multiple independent contact regions between the same species allow to determine the relative importance of intrinsic and extrinsic factors in the evolution of hybrid zones and thus, parallelism in hybridization outcomes. In this study, we take advantage of two hybrid regions between the damselfly species Ischnura elegans and I. graellsii in Spain to measure: i) the extent of parallelism across geographic hybridization replicates, and what factors (intrinsic and extrinsic) drive that variation; and ii) if hybridization has an impact on the ability of species to expand their ranges. RAD sequencing was used to generate 5,702 SNPs to quantify population diversity and population differentiation, and a subset of 381 species-specific SNPs to analyze genotypic composition (individual ancestry and the proportion of individuals in different hybrid classes Our individual ancestry results showed on-going hybridization and introgression with different admixture-class distributions between hybrid regions and between populations explained by i) species proportions, ii) time elapsed since colonization, and iii) asymmetric and reinforced prezygotic barriers and Batson Dobzhansky and Müller (BDM) hybrid incompatibilities, and indicated a role of hybridization as a facilitator of species range expansions. Our study highlights the value of studying complex hybrid zones to gain insights into microevolutionary processes.

Testing the predictions of reinforcement: long-term empirical data from a damselfly mosaic hybrid zone

“…1). This sympatry zone is a mosaic hybrid zone in which the frequencies of I. elegans and I. graellsii vary between populations and thus in their degrees of introgression (Sánchez-Guillén et al 2023). First records of I. elegans in the sympatric zone come from 1980 in Louro (both species), 1987 in Doniños (only I. elegans ) and 1995 in Foz (both species and hybrids).…”

“…Currently, these populations mainly consist of introgressed populations of I. elegans or introgressed I. graellsii , and only one of these populations, Louro, from which I. elegans was removed because of salinization of the lagoon in 2010, was after that recolonized in 2013 by both species, and displays different degrees of genetic admixture (introgressed, hybrids, backcrosses, etc. ; Sánchez-Guillén et al 2023). Although the sympatric region has only one hybrid population (Louro, since 2013), we expected to find evidence of reinforcement: firstly, because included populations have recently experienced hybridization, resulting in some cases with the local extinction of I. graellsii (Laxe, Doniños, Louro, Foz; Table S1), and in other cases the local extinction of I. elegans (e.g., Corrubedo complex; Table S1).…”

“…1), are a powerful model system to study the evolution of RI. The expansion of I. elegans has resulted in a mottled hybrid region, with two secondary contact zones (Sánchez-Guillén et al 2011, 2023). Mosaic and mottled hybrid zones, i.e., sympatric areas consisting of patches of alternating populations of each parental species and admixed populations (Rand and Harrison 1989), are ideal natural testbeds to study the evolution of reinforcement, for instance, its repeatability across multiple contact areas within a hybrid zone (Cain et al 1999; Hoskin and Higgie 2013).…”

“…Mosaic and mottled hybrid zones, i.e., sympatric areas consisting of patches of alternating populations of each parental species and admixed populations (Rand and Harrison 1989), are ideal natural testbeds to study the evolution of reinforcement, for instance, its repeatability across multiple contact areas within a hybrid zone (Cain et al 1999; Hoskin and Higgie 2013). This is the case of the north-west Spanish hybrid zone, which is characterized by having introgressed populations of each parental species and hybrid populations in which most individuals display different degrees of introgression, i.e., a unimodal distribution (Sánchez-Guillén et al 2023). Theory predicts that when sympatric speciation occurs, disruptive selection (such as reinforcement) should convert a unimodal distribution of genotypes to a bimodal one (Kondrashov et al 1998; Jiggins and Mallet 2000).…”

“…While isolation is almost complete in crosses of I. graellsii males and I. elegans females owing to mechanical incompatibilities, hybridization usually occurs in the opposite direction (Monetti et al 2002; Sánchez-Guillén et al 2012). The incomplete RI, the frequency distribution of the hybrid classes (Sánchez-Guillén et al 2023), the colonization and recolonization events, and the exceptional long-distribution data on this system all indicate that this system is a good candidate example to evaluate reinforcement.…”