Species delimitation beyond phylogenomics: integrative approaches reveal gentoo penguin speciation

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.