Ancestral Hybridization Yields Evolutionary Distinct Hybrids Lineages and Species Boundaries in Crocodiles, Posing Unique Conservation Conundrums

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.

High levels of population genetic differentiation in the American crocodile (Crocodylus acutus)

“…As a widespread species living across a diversity of fresh and brackish water habitats, able to move long distances across saltwater, the American crocodile has been often considered "homogenous" across its range. With most research focusing on hybrid zones (6,8,11,16,34), our study contributes to current debates on the taxonomic complexity of C. acutus (25,35) Overall, our findings improve our understanding of populations of C. acutus across seven countries and provide sound evidence of genetic structuring with direct consequences into management of local, unique populations.…”

“…Additionally, future studies should aim at using whole-genome sequencing to resolve population structuring further and to understand the phylogenetic evolution of the American crocodile and its relationships with other crocodilian species in the Americas and the Insular Caribbean. Finally, as research looks deeper into C. acutus lineages across its range and suggests the occurrence of potential cryptic species as a result of ancient hybridization and other evolutionary processes (25,35) our study aims at providing population-level data to inform current management and conservation as we continue our debate into C. acutus species designations.…”

“…In fact, hybridization between Cuban and American crocodiles in Cuba seems to have taken place both historically and in recent times (6). Similarly, ancestral and present hybridization has occurred between the American and Morelet's crocodiles in the Yucatan Peninsula (8,35). Regardless of potential evolutionary explanations for haplotype origins, the geographic distribution of C. acutus haplotypes suggests that strong genetic structuring shaped haplotype identities, followed by differences in haplotype frequencies.…”

High levels of population genetic differentiation in the American crocodile (Crocodylus acutus)

“…These clusters are usually defined considering habitat types within the species range, local conservation status, threats, enforcement, and legislation [19,31], as well as patterns of genetic variation within and among subpopulations. The majority of the work on C. acutus genetic variation has focused on zones where it can hybridize in the wild with C. rhombifer and C. moreletti [7,9,12,13,32,33]. Though information about genetic differentiation has been used as a tool for delineating local management units on some species of Crocodylus [34], there is still a need to incorporate population-level genetic information into conservation planning for many species of crocodilians, including the American crocodile.…”

“…C. acutus populations along the Pacific coast of Costa Rica exhibited small to moderate levels of inbreeding and significant levels of population differentiation potentially attributed to the lack of connectivity between some localities and the occurrence of population bottlenecks in the past [37]. In addition, Pacheco et al [33] extensive sampling throughout Mexico revealed several unique lineages as a result of historical and present hybridization between C. acutus and C moreletti. In parallel to C. acutus' species designation debates [33,36], it is imperative to strengthen the comparative research of extant populations to inform local and regional management and incorporate lacking information into the broader species assessment.…”