Unraveling the genomic landscape of Campylorhynchus wrens along western Ecuador's precipitation gradient: Insights into hybridization, isolation by distance, and isolation by the environment

Abstract

Environmental gradients have the potential to influence genetic differentiation among populations ultimately leading to allopatric speciation. However, environmental gradients can also facilitate hybridization between closely related taxa. We investigated a putative hybrid zone in western Ecuador, involving two polytypic wren species (Aves: Troglodytidae), Campylorhynchus zonatus and C. fasciatus. Our study addressed two primary questions: (1) Is there evidence of population structure and genetic admixture between these taxa in western Ecuador? and (2) What are the relative contributions of isolation by distance and isolation by the environment to the observed genetic differentiation along the environmental gradient in this region? We analyzed 4409 single-nucleotide polymorphisms (SNPs) from 112 blood samples sequenced using ddRadSeq and a de novo assembly. The optimum number of genetic clusters ranged from 2 to 4, aligning with geographic origins, known phylogenetics, and physical or ecological constraints. We observed notable transitions in admixture proportions along the environmental gradient in western Ecuador between C. z. brevirostris and the northern and southern genetic clusters of C. f. pallescens. Genetic differentiation between the two C. f. pallescens populations could be attributed to an unreported potential physical barrier in central western Ecuador, where the proximity of the Andes to the coastline restricts lowland habitats, limiting dispersal and gene flow, especially among dry-habitat specialists. The observed admixture in C. f. pallescens suggests that this subspecies may be a hybrid between C. z. brevirostris and C. fasciatus, with varying degrees of admixture in western Ecuador and northwestern Peru. We found evidence of isolation by distance, while isolation by the environment was less pronounced but still significant for annual mean precipitation and precipitation seasonality. This study enhances our understanding of avian population genomics in tropical regions.

Keywords: Campylorhynchus; hybridization; isolation by distance; isolation by the environment.

FIGURE 1

Sampling sites and distribution ranges of Campylorhynchus zonatus and C. fasciatus. Background colors show the AMP gradient in the region. Black triangle shows the climatic transition and the contact zone of these species.

FIGURE 2

Spatial principal component analysis (sPCA) plot for Campylorhynchus zonatus and C. fasciatus populations from western Ecuador and northern Peru, derived from ddRADSeq and de novo assembly data, excluding samples exhibiting a missing data rate exceeding 25% per individual. Each data point represents a single individual. The polygons delineate groups of individuals according to their subspecies designations based on Ridgely and Greenfield (2001), while the dot colors correspond to the genetic clusters assigned by the STRUCTURE software analysis when K = 4. The sPCA plot reveals that the genetic clusters largely align with the subspecies designations, although some degree of overlap on PC1 is observed between C. f. fasciatus and C. f. pallescens South, suggesting potential gene flow.

FIGURE 3

Population structure and admixture patterns in Campylorhynchus zonatus brevirostris and C. fasciatus along western Ecuador and northern Peru based on ddRADseq data and de novo assembly. STRUCTURE results showing individual admixture proportions for K = 2–4 genetic clusters. Each vertical bar represents an individual, ordered by sampling location from north to south, with locations separated by black vertical lines. Horizontal white lines indicate ancestry probabilities of 0.1 and 0.9. Distinct genetic clusters correspond to C. z. brevirostris, C. f. pallescens (North and South), and C. f. fasciatus.

FIGURE 4

The HI values for Campylorhynchus zonatus brevirostris and C. fasciatus individuals across their geographic ranges. Each vertical bar represents the HI estimate for an individual, color‐coded by sampling locality. Individuals are ordered latitudinally from northernmost (left) to southernmost (right) sites. Parental C. z. brevirostris and C. fasciatus individuals have HI values of 0 and 1, respectively. Intermediate values indicate admixed ancestry between the two species. Hybrid indices were estimated using the INTROGRESS R package based on ddRADseq data and the de novo assembly.