Abstract

Interspecific hybridization can lead to adaptation and speciation, especially in the context of recent radiations. The emblematic Crocodylus (true crocodiles) is the most broadly distributed, ecologically diverse, and species-rich crocodylian genus. Nonetheless, their within-species evolutionary processes are poorly resolved mainly due to their potential for hybridization. Notably, the evolutionary outcomes when hybridization is ancient and involves long-lived species, like crocodiles, remain largely unexplored. Here, we evaluate the genomic admixture between the American (Crocodylus acutus) and the Morelet’s (Crocodylus moreletii) species, and demonstrate that this hybridization system challenges the definition of species boundaries and poses a triple conservation conundrum: what has been recognized as C. acutus is actually two distinct species, therefore its taxonomic reassessment is needed; we identified two evolutionary distinct hybrids lineages, which are genetically discernible from the parental species; the remaining C. moreletii populations evidence its likely extinction as a species and/or evolution via hybridization. Hence, the crocodiles’ distinct species and hybrids lineages warrant recognition and need urgent conservation efforts.

Highlights

  • Since Darwin, hybridization has intrigued evolutionary biologists, recognized as a regular occurrence in nature and a significant source of variation (Roberts, 1919); a means for species to acquire beneficial alleles and the potential to adapt, contributing to the divergence and speciation of lineages (Mallet, 2007; Abbott et al, 2013; Sardell and Uy, 2016; Gompert et al, 2017)

  • We explore the following key questions: (i) Can we elucidate the evolutionary relationships between and within these crocodile species? (ii) When did the hybridization process between Crocodylus acutus and C. moreletii start? (iii) Can different lineages be distinguished, both in terms of parental and hybrid individuals? (iv) Can species boundaries be defined in this hybridization system? Our ultimate goal was to discern if hybridization could be leading to the differentiation of evolutionary lineages and, if so, what would be the conservation consequences and protection policy challenges

  • The Gulf of Mexico and the Pacific populations form five distinguishable separate clusters (Figures 2C,D, and Figures S2B,C): two different groups of nonadmixed C. acutus from the Pacific, non-admixed C. acutus from the Caribbean islands, non-admixed C. moreletii from the Gulf of Mexico, and hybrids predominantly from the Gulf of Mexico and within some Pacific localities. This pattern is highly concordant with the hybrid index results (h): a few non-admixed and isolated individuals for both C. moreletii and C. acutus and a range of hybrids throughout the entire distribution (Figure 2B, and Figure S2A)

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Summary

Introduction

Since Darwin, hybridization has intrigued evolutionary biologists, recognized as a regular occurrence in nature and a significant source of variation (Roberts, 1919); a means for species to acquire beneficial alleles and the potential to adapt, contributing to the divergence and speciation of lineages (Mallet, 2007; Abbott et al, 2013; Sardell and Uy, 2016; Gompert et al, 2017). The evolutionary outcomes when hybridization is ancient and involves long-lived species with deep divergences, like crocodiles, remain largely unexplored. In such systems, the likely prediction would be a hybrid zone that is shaped by multiple episodes of primary divergence and secondary contact, reflecting both recent and ancient hybridization, with different outcomes including wide admixture zones, genetic swamping of one species by another, or reproductive isolation and hybrid speciation. Unraveling the dynamics and consequences of such introgression systems can enrich our understanding of the role of hybridization in shaping biodiversity, and help elucidate the evolutionary relationships within species

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