Heterozygosity levels and historical demography
Current level of intraspecific heterozygosity is a relevant parameter to
determine the adaptive capacity of a population (or species) (Ørsted,
Hoffmann, Sverrisdóttir, Nielsen, & Kristensen, 2019). Since the
Balearic shearwater is categorised as Critically Endangered by the IUCN,
we could naively expect low heterozygosity levels in the species when
compared to other Procellariiformes. However, the fossil record suggests
that the Balearic shearwater had a very large population
(>30.000 pairs) until the arrival of human settlers in the
Balearic Islands (Alcover, J.A., Bover, P., Seguí, 1991), which hunted
shearwaters (Ramis, 2018) and introduced invasive mammals that also
predated on them (Pinya & Carretero, 2011). In line with Genovart, Oro,
Juste, & Bertorelle, (2007) results using mtDNA markers, we observed
relatively high genome-wide heterozygosity levels, suggesting that the
very recent demographic decline in the species is not yet visible in its
genetic diversity.
Regarding the historical demography, our PSMC’ analysis shows an
increase in N e in the Balearic shearwater from
around 1 Mya to later expand to reach high population sizes, until
around 150,000 ya, when it suddenly suffered a sharp decline, resulting
in lower N e values maintained until 10,000 years
ago. Since current PSMC’ analysis is based on the analysis of a single
genome, we could not reliably infer more recent events (Schiffels &
Wang, 2020). Pimiento et al., 2017 had shown that the Plio-Pleistocene
eustatic variations resulted in a loss of neritic zones as sea level
regressed, this may represent a loss of coastal habitat availability,
which added to other oceanographic alterations (changes in ocean
circulation or productivity) may have been the drivers of great
population losses in marine megafauna, including seabirds. In the case
of the Balearic shearwater, the PSMC’ analysis shows an abrupt decay ofN e associated with a long period of low sea level
during the Penultimate Glacial Period (~194-135 kya)
which may have resulted in an important loss of neritic zones.
Here, we have observed a negative correlation between heterozygosity and
body size within the Procellariiformes, where small-bodied species
(O. oceanicus , F. grallaria , H. tethys and P.
urinatrix ) have higher heterozygosities than large-bodied species
(F. glacialis , C. borealis , P. mauretanicus andT. chlororhynchos ). Although controversial, contrasting
heterozygosity levels between species with different body-sizes has also
been reported in different species including Procellariiformes (Estandia
et al. 2021; and references therein). Since body-size also correlates
with population size and with other life-history traits, current data
does not allow to determine the biological meaning of such correlation
effect (Estandía et al., 2021; Mackintosh et al., 2019).
In view of the critical population declines affecting the Balearic
shearwater populations, understanding its impacts on current genetic
diversity of the species and among colonies will be crucial to assess
the conservation status of the Balearic shearwater. Future ongoing
research, using a more powerful population genomics approach, will allow
to reconstruct the most recent demographic history of the species and to
test the fossil-based hypotheses of a recent loss of population due to
human colonization of the island, as well as why heterozygosity values
have not decayed.