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.