Genomic evidence of recent hybridization between sea turtles at Abrolhos Archipelago and its association to low reproductive output

Abstract

Hybridization between sea turtle species occurs with particularly high frequency at two adjacent nesting areas in northeastern Brazil. To understand the outcomes of hybridization and their consequences for sea turtle conservation, we need to evaluate the extent of hybridization occurrence and possible deleterious effects in the hybrid progeny. Thus, we investigated the hypothesis of the existence of a new hybrid spot offshore of Brazil’s northeastern coast. The Abrolhos Archipelago is surrounded by the largest and richest coral reefs in the South Atlantic and is known to be a nesting site for loggerhead turtles (Carettacaretta). In this study, we performed a multidisciplinary investigation into levels of hybridization in sea turtles and their reproductive output in the Abrolhos beaches. Genetic data from mitochondrial DNA (mtDNA) and six autosomal markers showed that there are first-generation hybrid females nesting in Abrolhos, resulting from crossings between hawksbill males (Eretmochelysimbricata) and loggerhead females, and backcrossed hatchlings from both parental species. The type and extent of hybridization were characterized using genomic data obtained with the 3RAD method, which confirmed backcrossing between F1 hybrids and loggerhead turtles. The reproductive output data of Abrolhos nests suggests a disadvantage of hybrids when compared to loggerheads. For the first time, we have shown the association between hybridization and low reproductive success, which may represent a threat to sea turtle conservation.

Evidence of backcross inviability and mitochondrial DNA paternal leakage in sea turtle hybrids

“…Given the lack of >F1 adults, the time passed since the first studies detected hybrids in the 1980s, combined with similar reproductive output of F1 and backcross hybrids compared to nonhybrid individuals, we expect that F2s (F1 × F1) and backcrosses have lower or much lower fitness related to genetic incompatibilities, with no or very rare opportunities to reach sexual maturity. A similar result of lack of >F1 adult hawksbill × loggerhead hybrids was also found in a smaller nesting population in Abrolhos Archipelago (~600 km south of Praia do Forte) where it was suggested a lower reproductive success among hatchlings of F1 hybrids when compared to loggerheads (Arantes, Ferreira, et al, 2020). In general, data from whole genomes indicated that ancient hybridization occurred in sea turtles (Vilaça et al, 2021) and left a signature in their genomes.…”

Evidence of backcross inviability and mitochondrial DNA paternal leakage in sea turtle hybrids

“…Given the lack of >F1 adults, the time passed since the first studies detected hybrids in the 1980s, combined with similar reproductive output of F1 and backcross hybrids compared to non-hybrid individuals, we expect that F2s (F1 x F1) and backcrosses have lower or much lower fitness related to genetic incompatibilities, with no or very rare opportunities to reach sexual maturity. A similar result of lack of >F1 adult hawksbill x loggerhead hybrids was also found in a smaller nesting population in Abrolhos Archipelago (~600 km south from Praia do Forte) where it was suggested a lower reproductive success among hatchlings of F1 hybrids when compared to loggerheads (Arantes, Ferreira, et al, 2020). In general, data from whole genomes indicated that ancient hybridization occurred in sea turtles (Vilaça et al, 2021) and left a signature in the modern genomes.…”

The genomic consequences of hybridization

“…In this review, we synthesize research into the consequences of admixture spanning different timescales and population histories of hybridization. The advent of inexpensive whole-genome sequencing has allowed for the detection of ancient hybridization events, adding to a rich literature of contemporary hybridization events ( Taylor et al, 2014 ; Salvatori et al, 2019 ; Grant et al, 2005 ; Chaturvedi et al, 2020 ; Arantes et al, 2020 ; Carling and Zuckerberg, 2011 ; Geraldes, 2014 ) and stable zones where hybridization has been ongoing for thousands of generations ( Teeter et al, 2008 ; Smith et al, 2013 ; De La Torre et al, 2015 ; Ramsey, 2003 ; Szymura and Barton, 1986 ; Shaw and Wilkinson, 1980 ; Sage, 1986 ; Bert and Arnold, 1995 ; Ruegg, 2008 ). The distinct timescales of different admixture events allow us to ask questions about both the early and late stages of genome evolution and stabilization following hybridization.…”

“…Much of our discussion focuses on a pulse model of hybridization, where an admixed population arose from two diverged populations at some point in time in the past, and hybridization has since stopped. While this model is an oversimplification in most cases, many scenarios of introgression can be well approximated by a pulse model ( Taylor et al, 2014 ; Salvatori et al, 2019 ; Grant et al, 2005 ; Chaturvedi et al, 2020 ; Arantes et al, 2020 ), which simplifies interpretation of the dynamics of genome stabilization following hybridization. For example, this model lends itself to evaluating how the genome stabilizes over time, which evolutionary processes occur shortly after initial gene exchange ( Schumer et al, 2018 ; Matute et al, 2020 ), and which occur over a longer time period ( Schumer et al, 2016 ; Sankararaman et al, 2016 ; Chaturvedi et al, 2020 ; Gompert et al, 2006 ; Trier et al, 2014 ).…”