Level of inbreeding and strategies to avoid relatedness in the population
Inbreeding was significant in this population (Fis =0.06, p_value < 0.001) and coupled with a higher relatedness than expected by chance. This indicates that these turtles breed non-randomly and overall do not avoid inbreeding. A similar situation was found by Horne et al. (2022) in a Hawaiian hawksbill turtle population, and was correlated with strong philopatry to nesting complexes less than 100 km apart. Here, the atoll of Tetiaroa has a total area of only 6 sq. km, but each female was found nesting on only one or two of the 11 islets surveyed (Supplementary Data 6). Such a level of male philopatry (< 1-2km) would be surprising given the scale, the absence of a swimming barrier around the island, and the capacity of males to connect rookeries (Bradshaw et al., 2018; Roberts et al., 2004).
The levels of relatedness observed could not be correlated with a loss of fitness when measuring clutch parameters. Philips et al. (2017) suggested that relatedness levels and parental multilocus heterozygosity can interact in both negative and positive ways in turtle populations and that relatedness alone does not explain levels of fitness, but investigating these interactions is beyond the scope of this study. None of the mating behaviour deduced from the parentage analysis (mating with multiple partners, breeding more frequently, or having a higher share of paternity in multipaternity clutches) seemed to efficiently mitigate inbreeding, as the relatedness of pairs involved in these behaviours was similar to the overall relatedness. This is in discordance with the inbreeding avoidance theory that predicts that populations would tend to avoid inbreeding with pre and postcopulatory mechanisms (Blouin and Blouin, 1988; Cornell and Tregenza, 2007; but see Szulkin et al., 2013). Inbreeding avoidance is suspected in a small population of leatherback turtles in the South West Atlantic (Vargas et al., 2022). On the contrary, mating choices in this population seem to be driven by other factors. At the scale of French Polynesia, three populations were identified regardless of their nesting islands and mitochondrial lineage (Dolfo et al., submitted). When including reconstructed male genotypes from Tetiaroa in this analysis, most of them belonged to the same “genetic population” as their female mates (Supplementary Data 8). However, in Tetiaroa, three distinct genetic populations coexist, indicating a deliberate selection of partners rather than random pairing. As proposed by the authors, these populations may be linked with phenotypical or ecotypical preferences in partner choice (e.g. carapace colour and shape) or may be conditioned to breeding grounds that occur irrespective of nesting islands. However, in Tetiaroa, breeding behaviours are observed in the vicinity of the island (Gaspar, pers. comm.), suggesting that breeders then nest on this island. Courtship is usually observed as a result of repetitive attempts by males, as females can also refuse mating (Booth and Peters, 1972). Green turtle courting behaviour should thus be investigated to further determine what may drive such a non-random mating choice.
Additionally, our results on multipaternity clutches contradict the ‘gene compatibility’ theory, as the dominant father in multipaternity clutches was more related to the female than the other male. Dominance in shares of multipaternity is thought to be linked with first male sperm precedence (Fitzsimmons, 1998). This, for example, is confirmed in nests 1415_ONE8 and 1415_ONE9. In these nests, the dominant male was found in all of the other nests earlier in the season (Table 4), while the non-dominant male was not found in any of the nests. Although the latter might have been missed in the early nests, this pattern may also reflect a second mating occurring later in the nesting season. In this case, multipaternity might mitigate inbreeding by mating with other partners when the first one has a high level of relatedness. This mechanism is observed in the Whites’ skink (Egernia whitii ), where females sometimes seek a second and less related partner outside their social group, which increases the offspring heterozygosity (While et al., 2014). In Chinese alligators (Alligator sinensis ), polyandry females mate with males that are less related to them than monogamy females, mitigating inbreeding in the population (Wang et al., 2017). To date, very few studies have explored relatedness in multiple paternity clutches of marine turtles (Phillips et al., 2013). This hypothesis therefore needs to be confirmed with a higher number of multipaternity clutches and deserves further investigations in other populations.