Extensive introgression among strongylocentrotid sea urchins revealed by phylogenomics

Abstract

Gametic isolation is thought to play an important role in the evolution of reproductive isolation in broadcast‐spawning marine invertebrates. However, it is unclear whether gametic isolation commonly evolves early in the speciation process or only accumulates after other reproductive barriers are already in place. It is also unknown whether gametic isolation is an effective barrier to introgression following speciation. Here, we used whole‐genome sequencing data and multiple complementary phylogenomic approaches to test whether the well‐documented gametic incompatibilities among the strongylocentrotid sea urchins have limited introgression. We quantified phylogenetic discordance, inferred reticulate phylogenetic networks, and applied the Δ statistic using gene tree topologies reconstructed from multiple sequence alignments of protein‐coding single‐copy orthologs. In addition, we conducted ABBA–BABA tests on genome‐wide single nucleotide variants and reconstructed a phylogeny of mitochondrial genomes. Our results revealed strong mito‐nuclear discordance and considerable nonrandom gene tree discordance that cannot be explained by incomplete lineage sorting alone. Eight of the nine species examined demonstrated a history of introgression with at least one other species or ancestral lineage, indicating that introgression was common during the diversification of the strongylocentrotid urchins. There was strong support for introgression between four extant species pairs (Strongylocentrotus pallidus ⇔ S. droebachiensis, S. intermedius ⇔ S. pallidus, S. purpuratus ⇔ S. fragilis, and Mesocentrotus franciscanus ⇔ Pseudocentrotus depressus) and additional evidence for introgression on internal branches of the phylogeny. Our results suggest that the existing gametic incompatibilities among the strongylocentrotid urchin species have not been a complete barrier to hybridization and introgression following speciation. Their continued divergence in the face of widespread introgression indicates that other reproductive isolating barriers likely exist and may have been more critical in establishing reproductive isolation early in speciation.

Selection shapes the genomic landscape of introgressed ancestry in a pair of sympatric sea urchin species

“…The percentage of bases introgressed rose to 5% overall and 6% in coding regions. These estimates of the proportion of the genome introgressed (1 -5 %) align with previous estimates for S. pallidus and S. droebachiensis (Glasenapp and Pogson, 2023). Summary statistics for the introgression tracts at both probability thresholds are provided in Supplementary Table S3, and information on all introgression tracts can be found in Supplementary Tables S4 and S5.…”

“…The strongylocentrotid sea urchin family stands out relative to other population genetic models for their massive effective population sizes, highly efficient selection, and high gene flow across ocean basins. Although the species are well-diverged (4.2 -19.0 mya), and natural hybrids are rare, many of the species show strong signals of historical introgression (Glasenapp and Pogson 2023). In our analysis of introgression between S. pallidus and S. droebachiensis, we found strong evidence for genome-wide selection against introgression, including two chromosomes depleted of introgression warranting further examination.…”

“…However, hybrids of S. pallidus and S. droebachiensis morphologically resemble S. pallidus as larvae and S. droebachiensis as adults, so the frequency of natural hybrids may be underestimated. Introgression between S. pallidus and S. droebachiensis has been previously detected (Addison and Hart 2005;Addison and Pogson 2009;Pujolar and Pogson 2011;Glasenapp and Pogson 2023).…”

“…Additionally, their high amounts of recombination (Brennan et al 2019) and lack of population structure (Palumbi and Wilson 1990;Palumbi and Kessing 1991) should promote the retention of introgressed ancestry. Several studies have documented introgression between a pair of recently-diverged, non-sister taxa that co-occur and hybridize in both the North Pacific and North Atlantic: S. pallidus and S. droebachiensis (Addison and Hart 2005;Addison and Pogson 2009;Pujolar and Pogson 2011;Glasenapp and Pogson 2023). However, the genomic regions showing signals of introgression have yet to be characterized.…”

Selection Shapes the Genomic Landscape of Introgressed Ancestry in a Pair of Sympatric Sea Urchin Species

“…The strongylocentrotid family of sea urchins is a compelling group for characterizing the genomic landscape of introgression. Extensive introgression has occurred among the strongylocentrotid urchins ( Glasenapp and Pogson 2023 ), and the purple sea urchin, Strongylocentrotus purpuratus (Stimpson), has a well-annotated reference genome and a long history of use as a model organism in fertilization and development studies. The selective histories of the single-copy protein-coding genes in this family have been formally characterized ( Kober and Pogson 2017 ), providing valuable context for interpreting introgression patterns.…”