Stable Species Boundaries Despite Ten Million Years of Hybridization in Tropical Eels

Abstract

1Genomic evidence is increasingly underpinning that hybridization between taxa is commonplace, 2 challenging our views on the mechanisms that maintain their boundaries. Here, we focus on seven 3 catadromous eel species (genus Anguilla), and use genome-wide sequence data from more than 450 4 individuals sampled across the tropical Indo-Pacific, morphological information, and three newly 5 assembled draft genomes to compare contemporary patterns of hybridization with signatures of 6 past gene flow across a time-calibrated phylogeny. We show that the seven species have remained 7 distinct entities for up to 10 million years, despite a dynamic scenario of incomplete isolation 8 whereby the current frequencies of hybridization across species pairs (over 5% of all individuals 9 were either F1 hybrids or backcrosses) contrast remarkably with patterns of past introgression. 10Based on near-complete asymmetry in the directionality of hybridization and decreasing frequencies 11 of later-generation hybrids, we identify cytonuclear incompatibilities and hybrid breakdown as two 12 powerful mechanisms that can support species cohesion even when hybridization has been pervasive 13 throughout the evolutionary history of entire clades. 14 Introduction 17The turn of the century has witnessed a paradigm shift in how we view the role of hybridization 18 for building up biological diversity. While hybridization was previously assumed to be spatially 19 restricted and confined to a small number of taxa, it became gradually recognized that incomplete 20 isolation of genomes is widespread across eukaryotes, with varied effects on adaptation and speci-21 ation (Mallet, 2005(Mallet, , 2007 Abbott et al., 2013; Taylor and Larson, 2019). More recently, this view 22 has been further fuelled by technical and analytical advances which enable the quantification of past 23 introgression, the genetic exchange through hybridization, across entire clades, revealing that it is 24 often the most rapidly radiating clades that experienced high frequencies of gene exchange (Meier 25 et al., 2017; Lamichhaney et al., 2018; Kozak et al., 2018; Edelman et al., 2018). This seemingly 26 paradoxical association between introgression and rapid species proliferation underlies a key ques-27 tion in evolutionary biology: How can species in diversifying clades be accessible for introgression 28 but nevertheless solidify their species boundaries? To answer this question, insights are required 29 into the mechanisms that gradually reduce the degree to which hybridization generates introgres-30 sion; however, these mechanisms are still poorly understood because contemporary hybridization 31 and past introgression have so far not been jointly studied and compared across multiple pairs of 32 animal species with different divergence times within a single clade.33 Teleost fish provide well-established model systems to reveal processes of diversification, includ-34 ing the impact of hybridization on speciation (e.g., Malinsky et al., 2018a; Hench et al. 2019).35 A partic...

Genetic signature of hybridization between Chinese spot‐billed ducks and domesticated ducks

“…However, the domestic genetic material moving into CSB does not imply that the CSB faces a genetic extinction threat as these segmentations are rarely fixed in CSB (Tables S5 and S7). The deleterious alleles that are introduce from domesticated ducks will possibly be eliminated by purifying selection (Juric et al 2016;Barth et al 2020). It is noteworthy that continuous and abundant release of domesticated animals greatly increases the chance of wild-domesticated hybridization and even backcrossing into their wild parental population, which may result in the genetic swamping of wild populations (Chazara et al, 2010;Lavretsky et al 2020).…”

Skin coloration and habitat preference of the freshwater Anguilla eels

“…Interestingly, recent study indicated that hybridization and gene exchange are pervasive in tropical eel species, but that these species have nevertheless remained distinct entities for several million years. Cytonuclear incompatibilities and hybrid breakdown may be powerful mechanisms which help maintaining species boundaries [49].…”

Contemporary Philosophy and Methods for Studying Speciation and Delimiting Species

“…These authors contend that species delimitations from multiple herpetological studies were unfounded because they represent arbitrary slices of clines or conjecture that hybrid zones are too wide for species to be valid. However, they ignore that hybridization across the tree of life is common, these species diverged during the Pleistocene or even earlier and have maintained independent evolutionary trajectories, and incomplete gene (lineage) sorting is one expectation of the speciation process (Wiley, 1978;Knowles and Carstens, 2007b;de Queiroz, 2007;Payseur and Rieseberg, 2016;Gompert et al, 2017;Barth et al, 2020;Moran et al, 2021).…”