Intrinsic and extrinsic drivers of shape variation in the albatross compound bill.

Albatross are the largest seabirds on Earth and have a suite of adaptations for their pelagic lifestyle. Rather than having a bill made of a single piece of keratin, Procellariiformes have a compound rhamphotheca, made of several joined plates. Drivers of the shape of the albatross bill have not been explored. Here we use three-dimensional scans of 61 upper bills from 12 species of albatross to understand whether intrinsic (species assignment & size) or extrinsic (diet) factors predict bill shape. Diet is a significant predictor of bill shape with coarse dietary categories providing higher R2 values than dietary proportion data. We also find that of the intrinsic factors, species assignment accounts for ten times more of the variation than size (72% versus 6.8%) and that there is a common allometric vector of shape change between all species. When considering species averages in a phylogenetic framework, there are significant Blomberg's K results for both shape and size (K = 0.29 & 1.10) with the first axis of variation having a much higher K value (K = 1.9), reflecting the split in shape at the root of the tree. The influence of size on bill shape is limited, with species assignment and diet predicting far more of the variation. The results show that both intrinsic and extrinsic factors are needed to understand morphological evolution.

Diving into a dead-end: asymmetric evolution of diving drives diversity and disparity shifts in waterbirds.

Diving is a relatively uncommon and highly specialized foraging strategy in birds, mostly observed within the Aequorlitornithes (waterbirds) by groups such as penguins, cormorants and alcids. Three key diving techniques are employed within waterbirds: wing-propelled pursuit diving (e.g. penguins), foot-propelled pursuit diving (e.g. cormorants) and plunge diving (e.g. gannets). How many times diving evolved within waterbirds, whether plunge diving is an intermediate state between aerial foraging and submarine diving, and whether the transition to a diving niche is reversible are not known. Here, we elucidate the evolutionary history of diving in waterbirds. We show that diving has been acquired independently at least 14 times within waterbirds, and this acquisition is apparently irreversible, in a striking example of asymmetric evolution. All three modes of diving have evolved independently, with no evidence for plunge diving as an intermediate evolutionary state. Net diversification rates differ significantly between diving versus non-diving lineages, with some diving clades apparently prone to extinction. We find that body mass is evolving under multiple macroevolutionary regimes, with unique optima for each diving type with varying degrees of constraint. Our findings highlight the vulnerability of highly specialized lineages during the ongoing sixth mass extinction.

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.

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.

Phylogeography of the Rufous Vanga and the role of bioclimatic transition zones in promoting speciation within Madagascar.

Madagascar is known as a biodiversity hotspot, providing an ideal natural laboratory for investigating the processes of avian diversification. Yet, the phylogeography of Madagascar's avifauna is still largely unexamined. In this study, we evaluated phylogeographic patterns and species limits within the Rufous Vanga, Schetba rufa, a monotypic genus of forest-dwelling birds endemic to the island. Using an integrative taxonomic approach, we synthesized data from over 4000 ultra-conserved element (UCE) loci, mitochondrial DNA, multivariate morphometrics, and ecological niche modeling to uncover two reciprocally monophyletic, geographically circumscribed, and morphologically distinct clades of Schetba. The two lineages are restricted to eastern and western Madagascar, respectively, with distributions broadly consistent with previously described subspecies. Based on their genetic and morphological distinctiveness, the two subspecies merit recognition as separate species. The bioclimatic transition between the humid east and dry west of Madagascar likely promoted population subdivision and drove speciation in Schetba during the Pleistocene. Our study is the first evidence that an East-West bioclimatic transition zone played a role in the speciation of birds within Madagascar.

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.

Hidden diversity of forest birds in Madagascar revealed using integrative taxonomy.

Madagascar is renowned as a global biodiversity hotspot with high levels of microendemism. However, there are few molecular phylogenetic studies of Malagasy birds, particularly for forest-dwelling species, signifying a substantial gap in current measures of species diversity in the absence of genetic data. We evaluated species limits and explored patterns of diversification within the genus Newtonia (Family Vangidae), a group of forest-dwelling songbirds endemic to Madagascar. Our modern systematics approach combined genomic, morphometric, and ecological niche data to analyze the evolutionary history of the group. Our integrative analysis uncovered hidden species-level diversity within N. amphichroa, with two deeply divergent and morphologically distinct lineages isolated in different regions of humid forest. We describe the southern lineage as a new species. Conversely, N. brunneicauda, which we initially hypothesized may harbor cryptic diversity owing to its large distribution spanning a range of habitats, was found to have no distinct lineages and shared haplotypes across much of its distribution. The contrasting diversification patterns between Newtonia lineages may be the result of their elevational tolerances. Newtonia brunneicauda has a broad habitat tolerance and elevational range that appears to have facilitated population expansion and gene flow across the island, limiting opportunities for diversification. On the other hand, N. amphichroa is found predominantly in mid-elevation and montane humid forests, a restriction that appears to have promoted speciation associated with climatic fluctuations during the Pleistocene. Our findings indicate that species diversity of Malagasy forest-dwelling birds may be greater than currently recognized, suggesting an urgent need for further studies to quantify biodiversity in Madagascar's rapidly disappearing native forests.

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.

Contrasting responses to a climate regime change by sympatric, ice-dependent predators.

BACKGROUND: Models that predict changes in the abundance and distribution of fauna under future climate change scenarios often assume that ecological niche and habitat availability are the major determinants of species' responses to climate change. However, individual species may have very different capacities to adapt to environmental change, as determined by intrinsic factors such as their dispersal ability, genetic diversity, generation time and rate of evolution. These intrinsic factors are usually excluded from forecasts of species' abundance and distribution changes. We aimed to determine the importance of these factors by comparing the impact of the most recent climate regime change, the late Pleistocene glacial-interglacial transition, on two sympatric, ice-dependent meso-predators, the emperor penguin (Aptenodytes forsteri) and Weddell seal (Leptonychotes weddellii). METHODS: We reconstructed the population trend of emperor penguins and Weddell seals in East Antarctica over the past 75,000 years using mitochondrial DNA sequences and an extended Bayesian skyline plot method. We also assessed patterns of contemporary population structure and genetic diversity. RESULTS: Despite their overlapping distributions and shared dependence on sea ice, our genetic data revealed very different responses to climate warming between these species. The emperor penguin population grew rapidly following the glacial-interglacial transition, but the size of the Weddell seal population did not change. The expansion of emperor penguin numbers during the warm Holocene may have been facilitated by their higher dispersal ability and gene flow among colonies, and fine-scale differences in preferred foraging locations. CONCLUSIONS: The vastly different climate change responses of two sympatric ice-dependent predators suggests that differing adaptive capacities and/or fine-scale niche differences can play a major role in species' climate change responses, and that adaptive capacity should be considered alongside niche and distribution in future species forecasts.

The influence of historical climate changes on Southern Ocean marine predator populations: a comparative analysis.

The Southern Ocean ecosystem is undergoing rapid physical and biological changes that are likely to have profound implications for higher-order predators. Here, we compare the long-term, historical responses of Southern Ocean predators to climate change. We examine palaeoecological evidence for changes in the abundance and distribution of seabirds and marine mammals, and place these into context with palaeoclimate records in order to identify key environmental drivers associated with population changes. Our synthesis revealed two key factors underlying Southern Ocean predator population changes; (i) the availability of ice-free ground for breeding and (ii) access to productive foraging grounds. The processes of glaciation and sea ice fluctuation were key; the distributions and abundances of elephant seals, snow petrels, gentoo, chinstrap and Adélie penguins all responded strongly to the emergence of new breeding habitat coincident with deglaciation and reductions in sea ice. Access to productive foraging grounds was another limiting factor, with snow petrels, king and emperor penguins all affected by reduced prey availability in the past. Several species were isolated in glacial refugia and there is evidence that refuge populations were supported by polynyas. While the underlying drivers of population change were similar across most Southern Ocean predators, the individual responses of species to environmental change varied because of species specific factors such as dispersal ability and environmental sensitivity. Such interspecific differences are likely to affect the future climate change responses of Southern Ocean marine predators and should be considered in conservation plans. Comparative palaeoecological studies are a valuable source of long-term data on species' responses to environmental change that can provide important insights into future climate change responses. This synthesis highlights the importance of protecting productive foraging grounds proximate to breeding locations, as well as the potential role of polynyas as future Southern Ocean refugia.

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.