Local prey shortages drive foraging costs and breeding success in a declining seabird, the Atlantic puffin.

As more and more species face anthropogenic threats, understanding the causes of population declines in vulnerable taxa is essential. However, long-term datasets, ideal to identify lasting or indirect effects on fitness measures such as those caused by environmental factors, are not always available. Here we use a single year but multi-population approach on populations with contrasting demographic trends to identify possible drivers and mechanisms of seabird population changes in the north-east Atlantic, using the Atlantic puffin, a declining species, as a model system. We combine miniature GPS trackers with camera traps and DNA metabarcoding techniques on four populations across the puffins' main breeding range to provide the most comprehensive study of the species' foraging ecology to date. We find that puffins use a dual foraging tactic combining short and long foraging trips in all four populations, but declining populations in southern Iceland and north-west Norway have much greater foraging ranges, which require more (costly) flight, as well as lower chick-provisioning frequencies, and a more diverse but likely less energy-dense diet, than stable populations in northern Iceland and Wales. Together, our findings suggest that the poor productivity of declining puffin populations in the north-east Atlantic is driven by breeding adults being forced to forage far from the colony, presumably because of low prey availability near colonies, possibly amplified by intraspecific competition. Our results provide valuable information for the conservation of this and other important North-Atlantic species and highlight the potential of multi-population approaches to answer important questions about the ecological drivers of population trends.

Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird.

Over evolutionary time, pathogen challenge shapes the immune phenotype of the host to better respond to an incipient threat. The extent and direction of this selection pressure depend on the local pathogen composition, which is in turn determined by biotic and abiotic features of the environment. However, little is known about adaptation to local pathogen threats in wild animals. The Gentoo penguin (Pygoscelis papua) is a species complex that lends itself to the study of immune adaptation because of its circumpolar distribution over a large latitudinal range, with little or no admixture between different clades. In this study, we examine the diversity in a key family of innate immune genes-the Toll-like receptors (TLRs)-across the range of the Gentoo penguin. The three TLRs that we investigated present varying levels of diversity, with TLR4 and TLR5 greatly exceeding the diversity of TLR7. We present evidence of positive selection in TLR4 and TLR5, which points to pathogen-driven adaptation to the local pathogen milieu. Finally, we demonstrate that two positively selected cosegregating sites in TLR5 are sufficient to alter the responsiveness of the receptor to its bacterial ligand, flagellin. Taken together, these results suggest that Gentoo penguins have experienced distinct pathogen-driven selection pressures in different environments, which may be important given the role of the Gentoo penguin as a sentinel species in some of the world's most rapidly changing environments.

Morphometric and genetic evidence for four species of gentoo penguin.

Gentoo penguins (Pygoscelis papua) are found across the Southern Ocean with a circumpolar distribution and notable genetic and morphological variation across their geographic range. Whether this geographic variation represents species-level diversity has yet to be investigated in an integrative taxonomic framework. Here, we show that four distinct populations of gentoo penguins (Iles Kerguelen, Falkland Islands, South Georgia, and South Shetlands/Western Antarctic Peninsula) are genetically and morphologically distinct from one another. We present here a revised taxonomic treatment including formal nomenclatural changes. We suggest the designation of four species of gentoo penguin: P. papua in the Falkland Islands, P. ellsworthi in the South Shetland Islands/Western Antarctic Peninsula, P. taeniata in Iles Kerguelen, and a new gentoo species P. poncetii, described herein, in South Georgia. These findings of cryptic diversity add to many other such findings across the avian tree of life in recent years. Our results further highlight the importance of reassessing species boundaries as methodological advances are made, particularly for taxa of conservation concern. We recommend reassessment by the IUCN of each species, particularly P. taeniata and P. poncetii, which both show evidence of decline.

Divergent selection and drift shape the genomes of two avian sister species spanning a saline-freshwater ecotone.

The role of species divergence due to ecologically based divergent selection-or ecological speciation-in generating and maintaining biodiversity is a central question in evolutionary biology. Comparison of the genomes of phylogenetically related taxa spanning a selective habitat gradient enables discovery of divergent signatures of selection and thereby provides valuable insight into the role of divergent ecological selection in speciation. Tidal marsh ecosystems provide tractable opportunities for studying organisms' adaptations to selective pressures that underlie ecological divergence. Sharp environmental gradients across the saline-freshwater ecotone within tidal marshes present extreme adaptive challenges to terrestrial vertebrates. Here, we sequence 20 whole genomes of two avian sister species endemic to tidal marshes-the saltmarsh sparrow (Ammospiza caudacutus) and Nelson's sparrow (A. nelsoni)-to evaluate the influence of selective and demographic processes in shaping genome-wide patterns of divergence. Genome-wide divergence between these two recently diverged sister species was notably high (genome-wide F ST = 0.32). Against a background of high genome-wide divergence, regions of elevated divergence were widespread throughout the genome, as opposed to focused within islands of differentiation. These patterns may be the result of genetic drift resulting from past tidal march colonization events in conjunction with divergent selection to different environments. We identified several candidate genes that exhibited elevated divergence between saltmarsh and Nelson's sparrows, including genes linked to osmotic regulation, circadian rhythm, and plumage melanism-all putative candidates linked to adaptation to tidal marsh environments. These findings provide new insights into the roles of divergent selection and genetic drift in generating and maintaining biodiversity.

Receding ice drove parallel expansions in Southern Ocean penguins.

Climate shifts are key drivers of ecosystem change. Despite the critical importance of Antarctica and the Southern Ocean for global climate, the extent of climate-driven ecological change in this region remains controversial. In particular, the biological effects of changing sea ice conditions are poorly understood. We hypothesize that rapid postglacial reductions in sea ice drove biological shifts across multiple widespread Southern Ocean species. We test for demographic shifts driven by climate events over recent millennia by analyzing population genomic datasets spanning 3 penguin genera (Eudyptes, Pygoscelis, and Aptenodytes). Demographic analyses for multiple species (macaroni/royal, eastern rockhopper, Adélie, gentoo, king, and emperor) currently inhabiting southern coastlines affected by heavy sea ice conditions during the Last Glacial Maximum (LGM) yielded genetic signatures of near-simultaneous population expansions associated with postglacial warming. Populations of the ice-adapted emperor penguin are inferred to have expanded slightly earlier than those of species requiring ice-free terrain. These concerted high-latitude expansion events contrast with relatively stable or declining demographic histories inferred for 4 penguin species (northern rockhopper, western rockhopper, Fiordland crested, and Snares crested) that apparently persisted throughout the LGM in ice-free habitats. Limited genetic structure detected in all ice-affected species across the vast Southern Ocean may reflect both rapid postglacial colonization of subantarctic and Antarctic shores, in addition to recent genetic exchange among populations. Together, these analyses highlight dramatic, ecosystem-wide responses to past Southern Ocean climate change and suggest potential for further shifts as warming continues.

Novel signals of adaptive genetic variation in northwestern Atlantic cod revealed by whole-genome sequencing.

Selection can create complex patterns of adaptive differentiation among populations in the wild that may be relevant to management. Atlantic cod in the Northwest Atlantic are at a fraction of their historical abundance and a lack of recovery within the Gulf of Maine has created concern regarding the misalignment of fisheries management structures with biological population structure. To address this and investigate genome-wide patterns of variation, we used low-coverage sequencing to perform a region-wide, whole-genome analysis of fine-scale population structure. We sequenced 306 individuals from 20 sampling locations in U.S. and Canadian waters, including the major spawning aggregations in the Gulf of Maine in addition to spawning aggregations from Georges Bank, southern New England, the eastern Scotian Shelf, and St. Pierre Bank. With genotype likelihoods estimated at almost 11 million loci, we found large differences in haplotype frequencies of previously described chromosomal inversions between Canadian and U.S. sampling locations and also among U.S. sampling locations. Our whole-genome resolution also revealed novel outlier peaks, some of which showed significant genetic differentiation among sampling locations. Comparisons between allochronic winter- and spring-spawning populations revealed highly elevated relative (FST ) and absolute (dxy ) genetic differentiation near genes involved in reproduction, particularly genes associated with the brain-pituitary-gonadal axis, which likely control timing of spawning, contributing to prezygotic isolation. We also found genetic differentiation associated with heat shock proteins and other genes of functional relevance, with complex patterns that may point to multifaceted selection pressures and local adaptation among spawning populations. We provide a high-resolution picture of U.S. Atlantic cod population structure, revealing greater complexity than is currently recognized in management. Our genome-scan approach likely underestimates the full suite of adaptive differentiation among sampling locations. Nevertheless, it should inform the revision of stock boundaries to preserve adaptive genetic diversity and evolutionary potential of cod populations.

Comparative population genomics reveals key barriers to dispersal in Southern Ocean penguins.

The mechanisms that determine patterns of species dispersal are important factors in the production and maintenance of biodiversity. Understanding these mechanisms helps to forecast the responses of species to environmental change. Here, we used a comparative framework and genomewide data obtained through RAD-Seq to compare the patterns of connectivity among breeding colonies for five penguin species with shared ancestry, overlapping distributions and differing ecological niches, allowing an examination of the intrinsic and extrinsic barriers governing dispersal patterns. Our findings show that at-sea range and oceanography underlie patterns of dispersal in these penguins. The pelagic niche of emperor (Aptenodytes forsteri), king (A. patagonicus), Adélie (Pygoscelis adeliae) and chinstrap (P. antarctica) penguins facilitates gene flow over thousands of kilometres. In contrast, the coastal niche of gentoo penguins (P. papua) limits dispersal, resulting in population divergences. Oceanographic fronts also act as dispersal barriers to some extent. We recommend that forecasts of extinction risk incorporate dispersal and that management units are defined by at-sea range and oceanography in species lacking genetic data.

The challenges of detecting subtle population structure and its importance for the conservation of emperor penguins.

Understanding the boundaries of breeding populations is of great importance for conservation efforts and estimates of extinction risk for threatened species. However, determining these boundaries can be difficult when population structure is subtle. Emperor penguins are highly reliant on sea ice, and some populations may be in jeopardy as climate change alters sea-ice extent and quality. An understanding of emperor penguin population structure is therefore urgently needed. Two previous studies have differed in their conclusions, particularly whether the Ross Sea, a major stronghold for the species, is isolated or not. We assessed emperor penguin population structure using 4,596 genome-wide single nucleotide polymorphisms (SNPs), characterized in 110 individuals (10-16 per colony) from eight colonies around Antarctica. In contrast to a previous conclusion that emperor penguins are panmictic around the entire continent, we find that emperor penguins comprise at least four metapopulations, and that the Ross Sea is clearly a distinct metapopulation. Using larger sample sizes and a thorough assessment of the limitations of different analytical methods, we have shown that population structure within emperor penguins does exist and argue that its recognition is vital for the effective conservation of the species. We discuss the many difficulties that molecular ecologists and managers face in the detection and interpretation of subtle population structure using large SNP data sets, and argue that subtle structure should be taken into account when determining management strategies for threatened species, until accurate estimates of demographic connectivity among populations can be made.

Dispersal in the sub-Antarctic: king penguins show remarkably little population genetic differentiation across their range.

BACKGROUND: Seabirds are important components of marine ecosystems, both as predators and as indicators of ecological change, being conspicuous and sensitive to changes in prey abundance. To determine whether fluctuations in population sizes are localised or indicative of large-scale ecosystem change, we must first understand population structure and dispersal. King penguins are long-lived seabirds that occupy a niche across the sub-Antarctic zone close to the Polar Front. Colonies have very different histories of exploitation, population recovery, and expansion. RESULTS: We investigated the genetic population structure and patterns of colonisation of king penguins across their current range using a dataset of 5154 unlinked, high-coverage single nucleotide polymorphisms generated via restriction site associated DNA sequencing (RADSeq). Despite breeding at a small number of discrete, geographically separate sites, we find only very slight genetic differentiation among colonies separated by thousands of kilometers of open-ocean, suggesting migration among islands and archipelagos may be common. Our results show that the South Georgia population is slightly differentiated from all other colonies and suggest that the recently founded Falkland Island colony is likely to have been established by migrants from the distant Crozet Islands rather than nearby colonies on South Georgia, possibly as a result of density-dependent processes. CONCLUSIONS: The observed subtle differentiation among king penguin colonies must be considered in future conservation planning and monitoring of the species, and demographic models that attempt to forecast extinction risk in response to large-scale climate change must take into account migration. It is possible that migration could buffer king penguins against some of the impacts of climate change where colonies appear panmictic, although it is unlikely to protect them completely given the widespread physical changes projected for their Southern Ocean foraging grounds. Overall, large-scale population genetic studies of marine predators across the Southern Ocean are revealing more interconnection and migration than previously supposed.

Population structure and phylogeography of the Gentoo Penguin (Pygoscelis papua) across the Scotia Arc.

Climate change, fisheries' pressure on penguin prey, and direct human disturbance of wildlife have all been implicated in causing large shifts in the abundance and distribution of penguins in the Southern Ocean. Without mark-recapture studies, understanding how colonies form and, by extension, how ranges shift is challenging. Genetic studies, particularly focused on newly established colonies, provide a snapshot of colonization and can reveal the extent to which shifts in abundance and occupancy result from changes in demographic rates (e.g., reproduction and survival) or migration among suitable patches of habitat. Here, we describe the population structure of a colonial seabird breeding across a large latitudinal range in the Southern Ocean. Using multilocus microsatellite genotype data from 510 Gentoo penguin (Pygoscelis papua) individuals from 14 colonies along the Scotia Arc and Antarctic Peninsula, together with mitochondrial DNA data, we find strong genetic differentiation between colonies north and south of the Polar Front, that coincides geographically with the taxonomic boundary separating the subspecies P. p. papua and P. p. ellsworthii. Using a discrete Bayesian phylogeographic approach, we show that southern Gentoos expanded from a possible glacial refuge in the center of their current range, colonizing regions to the north and south through rare, long-distance dispersal. Our findings show that this dispersal is important for new colony foundation and range expansion in a seabird species that ordinarily exhibits high levels of natal philopatry, though persistent oceanographic features serve as barriers to movement.

Too much of a good thing: sea ice extent may have forced emperor penguins into refugia during the last glacial maximum.

The relationship between population structure and demographic history is critical to understanding microevolution and for predicting the resilience of species to environmental change. Using mitochondrial DNA from extant colonies and radiocarbon-dated subfossils, we present the first microevolutionary analysis of emperor penguins (Aptenodytes forsteri) and show their population trends throughout the last glacial maximum (LGM, 19.5-16 kya) and during the subsequent period of warming and sea ice retreat. We found evidence for three mitochondrial clades within emperor penguins, suggesting that they were isolated within three glacial refugia during the LGM. One of these clades has remained largely isolated within the Ross Sea, while the two other clades have intermixed around the coast of Antarctica from Adélie Land to the Weddell Sea. The differentiation of the Ross Sea population has been preserved despite rapid population growth and opportunities for migration. Low effective population sizes during the LGM, followed by a rapid expansion around the beginning of the Holocene, suggest that an optimum set of sea ice conditions exist for emperor penguins, corresponding to available foraging area.

A reversal of fortunes: climate change 'winners' and 'losers' in Antarctic Peninsula penguins.

Climate change is a major threat to global biodiversity. Antarctic ecosystems are no exception. Investigating past species responses to climatic events can distinguish natural from anthropogenic impacts. Climate change produces 'winners', species that benefit from these events and 'losers', species that decline or become extinct. Using molecular techniques, we assess the demographic history and population structure of Pygoscelis penguins in the Scotia Arc related to climate warming after the Last Glacial Maximum (LGM). All three pygoscelid penguins responded positively to post-LGM warming by expanding from glacial refugia, with those breeding at higher latitudes expanding most. Northern (Pygoscelis papua papua) and Southern (Pygoscelis papua ellsworthii) gentoo sub-species likely diverged during the LGM. Comparing historical responses with the literature on current trends, we see Southern gentoo penguins are responding to current warming as they did during post-LGM warming, expanding their range southwards. Conversely, Adélie and chinstrap penguins are experiencing a 'reversal of fortunes' as they are now declining in the Antarctic Peninsula, the opposite of their response to post-LGM warming. This suggests current climate warming has decoupled historic population responses in the Antarctic Peninsula, favoring generalist gentoo penguins as climate change 'winners', while Adélie and chinstrap penguins have become climate change 'losers'.