Introduction
The genomic sequence of a species accumulates valuable information on
the evolutionary history, including demographic and selective events,
and on the evolution of genes and traits (Feng et al., 2020; Foote et
al., 2015; Jarvis et al., 2014; Nadachowska-Brzyska, Li, Smeds, Zhang,
& Ellegren, 2015), information that it is also crucial for the emerging
field of conservation genomics (Allendorf, 2017). The genetic diversity
within a species represents a reservoir of adaptive variation that can
help populations to cope with environmental variability (Dussex et al.,
2021). Understanding the processes that shape genetic diversity and its
distribution pattern within species is paramount to assess the
conservation status or the factors responsible for a species decline
(Brüniche-Olsen, Kellner, Belant, & DeWoody, 2021) (Wang et al., 2021).
This knowledge can inform the proposal of effective conservation and
management plans, as for instance the definition of management units
(Funk, McKay, Hohenlohe, & Allendorf, 2012). In this context,
next-generation sequencing (NGS) techniques allow the analysis of an
increased density of markers across the genome, providing unprecedented
accuracy in the estimations of population genetic parameters relevant
for scientific-based conservation recommendations (Supple & Shapiro,
2018).
Among the Critically Endangered species listed by the IUCN Red List
(IUCN 2021), we find the Balearic shearwater (Puffinus
mauretanicus Lowe, 1921) (Figure 1a) belonging to the most diverse
order of seabirds, the Procellariiformes. This order has a worldwide
distribution and comprises more than 140 species (IUCN 2021) in four
families: petrels and shearwaters (Procellariidae); northern storm
petrels (Hydrobatidae); southern storm petrels (Oceanitidae) and
albatrosses (Diomedeidae). All species show many morphological,
physiological and life history traits associated with their adaptation
to a pelagic lifestyle. They are long-lived with deferred sexual
maturity, low fecundity (all lay a single egg), colonial breeders,
socially (and mostly sexually) monogamous, highly phylopatric and with
prominent salt gland at the base of the bill, adaptations for underwater
vision to fish as well as a particularly acute sense of smell, among
other traits (Brooke, 2004). Within this apparent homogeneity, the group
shows a large variation in body mass and lifestyles, ranging from 20g to
15kg, from bodies shaped for diving (e.g. short strong wings used for
wing-propelled diving) to those prepared for an extremely vagile
lifestyle (thin elongated wings) and from a continuous flapping to
dynamic soaring flight modes. Currently, their phylogenetic
relationships present some conflicting issues (Estandía et al., 2021;
Hackett et al., 2008), such as the position of albatrosses, whether
storm petrels (Families Hydrobatidae and Oceanitidae) constitute a
monophyletic group, and whether diving-petrels (genusPelecanoides ) should be considered an independent family from
Procellariidae.
The Balearic shearwater is a medium-sized pelagic seabird endemic to the
Balearic Islands. Its population size is undergoing a fast annual
decline of 7.4-14% (Genovart et al., 2016; Oro, Aguilar, Igual, &
Louzao, 2004) mostly due to bycatch in longline fisheries and predation
by invasive mammals in the colonies (Arcos, Louzao, & Oro, 2008;
Louzao, Arcos, Hyrenbach, Sola, & Oro, 2004; Martí & Ruiz, 2004).
Currently, it has a reduced number of breeding pairs (estimated asca. 3,200, Arcos, 2011, with a total population size up to 30,000
individuals due to the vast contingent of floaters (Arcos et al., 2012;
Arroyo et al., 2016). Genetic studies based on mtDNA and microsatellites
found that this species has low levels of genetic diversity and high
inbreeding coefficients (Genovart, Juste, Contreras-Díaz, & Oro, 2012).
Although local inbreeding and natal philopatry can contribute to a
reduction in population size, the actual worst menace for the species
comes from human activities, and a population viability study based on
demographic modeling predicted that the species would become extinct by
2070 (Genovart et al., 2016).
Indeed, a population viability study based on demographic modeling
predicted that the species would become extinct by 2070 (Genovart et
al., 2016). Moreover, studies based on mitochondrial markers (Genovart,
Juste, & Oro, 2005) and also on morphology and migratory behaviour
(Austin et al., 2019), suggested a possible ongoing hybridization and
introgression process between Balearic and Mediterranean (P.
yelkouan ) shearwaters, which may represent an additional threat for the
species.
Here, we (1) provide a high-quality reference genome for the Balearic
shearwater along its structural and functional annotations; (2) estimate
genome-wide heterozygosity and the historical demography of the species
by performing Multiple Sequentially Markovian Coalescent (MSMC)
analyses; (3) revisit the phylogeny of the order by using this genome
together with seven additional Procellariiformes genomes released by the
B10K (Feng et al., 2020), and (4) uncover genes putatively involved in
Procellariiformes adaptation to pelagic life. The high-quality genome of
the most endangered seabird in Europe presented here will be the base
for further population-based conservation genomics studies.