Reconstructing hybridization events between sea turtle species separated by 30 million years: genomic patterns and evolutionary consequences

Project Information

TurtleHyb

Grant agreement ID: 844756

DOI

10.3030/844756

Project closed

EC signature date 12 April 2019

Start date 1 October 2019

End date 28 May 2022

Funded under

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Total cost

€ 183 473,28

EU contribution

€ 183 473,28

Coordinated by

UNIVERSITA DEGLI STUDI DI FERRARA
Italy

Periodic Reporting for period 1 - TurtleHyb (Reconstructing hybridization events between sea turtle species separated by 30 million years: genomic patterns and evolutionary consequences)

Reporting period: 2019-10-01 to 2021-09-30

Summary of the context and overall objectives of the project

Hybridization is a natural experiment of new genomic combinations. The encounter of two genomes that have been evolving separately will bring together untested allelic combinations that are usually unfavorable1 resulting in reduced hybrid viability or fertility. Whole genome studies combined with cutting-edge statistical analysis is increasingly showing that past hybridization events were common, where introgressed loci derived from these ancient events may still be segregating in the genomes of many species.
Sea turtles are truly amazing animals that have been swimming in the oceans since dinosaurs roamed the Earth. These endangered, ancient species have a fascinating hybridization system, as they are one of the oldest lineages known to naturally hybridize and generate viable and fertile offspring. Among all known hybrid combinations, species spanning phylogenetic divergence times from 15 million years (my) up to 48 my can still hybridize. As a comparison, within primates, these divergences are equivalent to the estimated splitting time between humans and gorillas to lemurs.
In a small region of Brazil two sea turtle species frequently hybridize. Previous studies estimated that 32-42% of nesting females morphologically identified as hawksbills (Eretmochelys imbricata) in Praia do Forte, Bahia State in Brazil are hybrids between hawksbills and loggerheads (Caretta caretta). This widespread hybridization process is possibly a consequence of overlapping nesting seasons, which also explained the directionality of the crossings, combined with few available mating partners due to recent population decreases as a consequence of hunting and poaching until the1980s7.
In endangered species, hybridization is often a consequence of declining population numbers. When species that have close or overlapping distribution and can still interbreed – decreases in size and consequently mating partners are rare, species hybridization is a likely outcome. In the project TurtleHyb, we studied the hybridization between sea turtle species in the South Atlantic Ocean. Our goal was 1) To test for putative past hybridization processes between Hawksbills and Loggerheads species; 2) Investigate if past population size changes could have triggered hybridization events; 3) Dissect the current hybridization events occurring in Brazil by identifying genomic regions associated with reproductive isolation by scanning the genomes of non-hybrid individuals for highly divergent regions.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

To reach our goals, we produced whole genome data for 33 individuals of four sea turtle species from Brazil and São Tomé, representing the southwestern and southeastern Atlantic Ocean, respectively. The sequenced samples comprised four sea turtle species (hawkskbills, loggerheads, olive ridleys and green sea turtles) and known loggerheads x hawksbill hybrids. We have used the newly generated data and state of the art statistics methods to identify past hybridization. The phylogenomic analysis run so far using showed a decline in effective population size (Ne) until approximately 250 thousand years ago. The Ne decrease is compatible with changes following the Mid Pleistocene transition and if similar, to alike decreases in population sizes, it might have triggered gene flow between species. Our results showed that there are indications of ancient gene flow between species. Our D-statistics were significant for several species’ combinations, with special significance to gene flow between loggerheads and hawksbills which are the main hybrid combination in Brazil (D=0.03 Z-score=33.17). Topology weighting showed several regions of the genome that had regions of discordant phylogenies, which could be associated with past hybridization between loggerheads x hawksbills and hawksbills x olive ridleys. When integrating our phylogeny results with methods like hybrid PSMC (hPSMC), we obtained an indication that gene flow continued long after species’ divergence. Thus, the contribution of ancestral gene flow was observed as discordances were present in the phylogenies, topology weighting, and significant D-statistics.
Part of the MSCA results have already been published in scientific journals (Vilaça et al 2021. Molecular Ecology Biology) and presented in conferences (Virtual Evolution 2021, 1st Italian Congress online on Marine Evolution in 2020 and 40th International Symposium of the Sea Turtle Society in 2022). We have also been active at communicating our research to the general public including local newspapers, online magazines, and social media.
Further analyses on all produced genomes are still ongoing and will report this past hybridization process in more details while also investigating the relationships between populations of sea turtle species across the South Atlantic Ocean. A second manuscript will report the findings from all data produced in this study. However, our project was heavily impacted by the pandemic which did not allow us to produce some of the originally planned data.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

In endangered species, hybridization can be a controversial phenomenon when considering management strategies. TurtleHyb studied species of conservation concern that frequently hybridize in Brazil to understand if this is an exclusively recent phenomenon, or if interspecies gene flow was part of these species’ evolutionary history. In addition, through our MSCA we described general patterns of genetic diversity, population structure past population dynamics and genome wide summary statistics. The detection of gene flow between sea turtle species by our genome-wide data indicates that signs of this ancient hybridization were inherited in their genomes over many generations. Further analysis will show if regions of the genome that show signs of hybridization have advantageous alleles and were positively selected. We also aim to elucidate if gene flow between sea turtle species is advantageous and can have positive impacts in their fitness. Our results also show that, similar to other marine species, gene flow was a part of sea turtles’ evolutionary history. This will contribute to a better understanding of the interplay between past and recent hybridization and its impacts in conservation strategies. This, while also having generated high-quality data for population-level genomes that will be available to the scientific community for further studies. In a changing world, climate warming may increase potential for hybridization due to altered reproductive interactions, changes in species ranges, and skewed sex ratios. Sea turtles are already being affected by climate change, and although hybridization can exacerbate extinction risk, it also has the potential to assist genetic rescue by increasing species’ adaptive potential. By integrating estimates of past and recent gene flow, our ultimate goal is to contribute to the preservation of these ancient long-living species.

Loggerhead sea turtle

Hawksbill sea turtle