Estimating the genetic and environmental components of variation in reproductive success is crucial to understanding the adaptive potential of populations to environmental change. To date, the heritability of lifetime reproductive success (fitness) has been estimated in a handful of wild animal population, mostly in mammals and birds, but has never been estimated for a marine species. The primary reason that such estimates are lacking in marine species is that most marine organisms have a dispersive larval phase, making it extraordinarily difficult to track the fate of offspring from one generation to the next.
In this study, Salles et al. [1] use an unprecedented 10 year data set for a wild population of orange clownfish (Amphiprion percula) to estimate the environmental, maternal and additive genetic components of life time reproductive success for the self-recruiting portion of the local population. Previous studies show that over 50% of juvenile clownfish recruiting to the population of clownfish at Kimbe Island (Kimbe Bay, PNG) are natal to the population. In other words, >50% of the juveniles recruiting to the population at Kimbe Island are offspring of parents from Kimbe Island. The identity and location of every adult clownfish in the Kimbe Island population was tracked over 10 years. At the same time newly recruiting juveniles were collected at regular intervals (biennially) and their parentage assigned with high confidence by 22 polymorphic microsatellite loci. Salles et al. then used a pedigree comprising 1735 individuals from up to 5 generations of clownfish at Kimbe Island to assess the contribution of every breeding pair of clownfish to self-recruitment within the local population. Because clownfish are site attached and live in close association with a host sea anemone, it was also possible to examine the contribution of reef location and host anemones species (either Heteractis magnifica or Stichodactyla gigantea) to reproductive success within the local population.
The study found that breeders from the eastern side of Kimbe Island, and mostly inhabiting S. gigantea sea anemones, produced more juveniles that recruited to the local population than breeders from other location around the island, or inhabiting H. magnifica. In fact, host anemone species and geographic location explained about 97% of the variance in reproductive success within the local population (i.e. excluding successful recruitment to other populations). By contrast, maternal and additive genetic effects explained only 1.9% and 1.3% of the variance, respectively. In other words, reef location and the species of host anemone inhabited had an overwhelming influence on the long-term contribution of breeding pairs of clownfish to replenishment of the local population. This overwhelming effect of the local habitat on reproductive success means that the population is potentially susceptible to rapid environmental changes - for example if S. giganta sea anemones are disproportionately susceptible to global warming, or reef habitats on the eastern side of the island are more susceptible to disturbance. By contrast, the small component of additive genetic variance in local reproductive success translated into low heritability and evolvability of lifetime reproductive success within the local population, as predicted by theory [2] and observed in some terrestrial species. Consequently, fitness would evolve slowly to environmental change.
Establishing the components of variation in fitness in a wild population of marine fishes is an astonishing achievement, made possible by the unprecedented long-term individual-level monitoring of the entire population of clownfish at Kimbe Island. A next step in this research would be to include other clownfish populations that are demographically and genetically connected to the Kimbe Island population through larval dispersal. It would be intriguing to establish the environmental, maternal and additive genetic components of reproductive success in the dispersing part of the Kimbe Island population, to see if this potentially differs among breeders who contribute more or less to replenishment within the local population.

References

[1] Salles, O. C., Almany, G. R., Berumen, M.L., Jones, G. P., Saenz-Agudelo, P., Srinivasan, M., Thorrold, S. R., Pujol, B., Planes, S. (2019). Strong habitat and weak genetic effects shape the lifetime reproductive success in a wild clownfish population. Zenodo, 3476529, ver. 3 peer-reviewed and recommended by Peer Community In Evolutionary Biology. doi: 10.5281/zenodo.3476529
[2] Fisher, R.A. (1930). The genetical theory of natural selection. Clarendon Press, Oxford, U.K.