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Dryad

Species delimitation beyond phylogenomics: integrative approaches reveal gentoo penguin speciation

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May 19, 2023 version files 49.15 MB

Abstract

Isolation and adaptation to new environments are important steps for reproductive isolation and consequently speciation. Seabirds have low phenotypic variation along their ranges in the absence of clear geographic or environmental barriers to dispersal. Despite the lacking visible phenotypic differences, the number of taxa for the gentoo penguin (Pygoscelis papua, Forster 1781) in the Southern Ocean has been under debate for the last decade, ranging from one to six different taxa. Here, we provide several lines of evidence from genomics, ecology, morphological data, and a complete systematic review that supports four distinctive gentoo penguin species, including the description of a new species. We also provide future niche projections for each of these species. Gentoo penguin genomes (n = 64) recover four main lineages: the northern gentoo (from South America), the southern gentoo (Antarctic Peninsula and maritime Antarctica, south of the Antarctic Polar Front, APF), the southeastern gentoo (from Kerguelen Islands), and the eastern gentoo (colonies located at lower latitudes north of the APF). Our analysis of selection across the genome recovered between 42 and 101 genes under selection for each of the four species, demonstrating that the four species are experiencing differing selective pressures that have caused them to diverge adaptively. The function of these genes affects traits that include reproduction, thermoregulation, osmoregulation, feed efficiency, and morphological variation. Morphological data were taken from museum individuals of all lineages, including from South Georgia gentoos, which have previously been considered a distinct taxon. Multivariate morphological comparisons of all pairs of lineages showed that the northern, southern, southeastern, and South Georgia gentoo penguins are morphologically distinct from each other (p < 0.05 for all pairwise comparisons), while the eastern lineage is intermediate in size and overlaps in morphospace with other lineages. This result also suggests that body size across latitudes is in direct contrast to Bergmann’s rule. Here, we describe the southeastern gentoo penguin from Kerguelen Island and confirm the taxonomic rank of gentoos from Macquarie Island and South Georgia Island as subspecies. Species distribution modelling suggests that climate change will expand the favourable space for the southern range expansion of the southern gentoo penguin but would result in a net loss of suitable habitats for compensatory niche shift relocation for the northern and southeastern gentoos. Despite this, amongst the three subantarctic species, the northern and southeastern gentoos possess high neutral and adaptive genetic diversity, including genes related to cold and heat response. This may represent a higher potential to evolve under environmental changes compared with the eastern gentoo penguin; therefore, the future resilience of each species remains uncertain. This study reinforces the urgent need for explicit recognition and protection of the four regional gentoo species based on their genetic, morphological, and ecological distinctiveness.