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.