Independent evolution of intermediate bill widths in a seabird clade.

Interspecific introgression can occur between species that evolve rapidly within an adaptive radiation. Pachyptila petrels differ in bill size and are characterised by incomplete reproductive isolation, leading to interspecific gene flow. Salvin's prion (Pachyptila salvini), whose bill width is intermediate between broad-billed (P. vittata) and Antarctic (P. desolata) prions, evolved through homoploid hybrid speciation. MacGillivray's prion (P. macgillivrayi), known from a single population on St Paul (Indian Ocean), has a bill width intermediate between salvini and vittata and could also be the product of interspecies introgression or hybrid speciation. Recently, another prion population phenotypically similar to macgillivrayi was discovered on Gough (Atlantic Ocean), where it breeds 3 months later than vittata. The similarity in bill width between the medium-billed birds on Gough and macgillivrayi suggest that they could be closely related. In this study, we used genetic and morphological data to infer the phylogenetic position and evolutionary history of P. macgillivrayi and the Gough medium-billed prion relative other Pachyptila taxa, to determine whether species with medium bill widths evolved through common ancestry or convergence. We found that Gough medium-billed prions belong to the same evolutionary lineage as macgillivrayi, representing a new population of MacGillivray's prion that originated through a colonisation event from St Paul. We show that macgillivrayi's medium bill width evolved through divergence (genetic drift) and independently from that of salvini, which evolved through hybridisation (gene flow). This represents the independent convergence towards a similarly medium-billed phenotype. The newly discovered MacGillivray's prion population on Gough is of utmost conservation relevance, as the relict macgillivrayi population in the Indian Ocean is very small.

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.

Subsistence practices, past biodiversity, and anthropogenic impacts revealed by New Zealand-wide ancient DNA survey.

New Zealand's geographic isolation, lack of native terrestrial mammals, and Gondwanan origins make it an ideal location to study evolutionary processes. However, since the archipelago was first settled by humans 750 y ago, its unique biodiversity has been under pressure, and today an estimated 49% of the terrestrial avifauna is extinct. Current efforts to conserve the remaining fauna rely on a better understanding of the composition of past ecosystems, as well as the causes and timing of past extinctions. The exact temporal and spatial dynamics of New Zealand's extinct fauna, however, can be difficult to interpret, as only a small proportion of animals are preserved as morphologically identifiable fossils. Here, we conduct a large-scale genetic survey of subfossil bone assemblages to elucidate the impact of humans on the environment in New Zealand. By genetically identifying more than 5,000 nondiagnostic bone fragments from archaeological and paleontological sites, we reconstruct a rich faunal record of 110 species of birds, fish, reptiles, amphibians, and marine mammals. We report evidence of five whale species rarely reported from New Zealand archaeological middens and characterize extinct lineages of leiopelmatid frog (Leiopelma sp.) and kakapo (Strigops habroptilus) haplotypes lost from the gene pool. Taken together, this molecular audit of New Zealand's subfossil record not only contributes to our understanding of past biodiversity and precontact Maori subsistence practices but also provides a more nuanced snapshot of anthropogenic impacts on native fauna after first human arrival.

Mitogenomes Uncover Extinct Penguin Taxa and Reveal Island Formation as a Key Driver of Speciation.

The emergence of islands has been linked to spectacular radiations of diverse organisms. Although penguins spend much of their lives at sea, they rely on land for nesting, and a high proportion of extant species are endemic to geologically young islands. Islands may thus have been crucial to the evolutionary diversification of penguins. We test this hypothesis using a fossil-calibrated phylogeny of mitochondrial genomes (mitogenomes) from all extant and recently extinct penguin taxa. Our temporal analysis demonstrates that numerous recent island-endemic penguin taxa diverged following the formation of their islands during the Plio-Pleistocene, including the Galápagos (Galápagos Islands), northern rockhopper (Gough Island), erect-crested (Antipodes Islands), Snares crested (Snares) and royal (Macquarie Island) penguins. Our analysis also reveals two new recently extinct island-endemic penguin taxa from New Zealand's Chatham Islands: Eudyptes warhami sp. nov. and a dwarf subspecies of the yellow-eyed penguin, Megadyptes antipodes richdalei ssp. nov. Eudyptes warhami diverged from the Antipodes Islands erect-crested penguin between 1.1 and 2.5 Ma, shortly after the emergence of the Chatham Islands (∼3 Ma). This new finding of recently evolved taxa on this young archipelago provides further evidence that the radiation of penguins over the last 5 Ma has been linked to island emergence. Mitogenomic analyses of all penguin species, and the discovery of two new extinct penguin taxa, highlight the importance of island formation in the diversification of penguins, as well as the extent to which anthropogenic extinctions have affected island-endemic taxa across the Southern Hemisphere's isolated archipelagos.

Ancient crested penguin constrains timing of recruitment into seabird hotspot.

New Zealand is a globally significant hotspot for seabird diversity, but the sparse fossil record for most seabird lineages has impeded our understanding of how and when this hotspot developed. Here, we describe multiple exceptionally well-preserved specimens of a new species of penguin from tightly dated (3.36-3.06 Ma) Pliocene deposits in New Zealand. Bayesian and parsimony analyses place Eudyptes atatu sp. nov. as the sister species to all extant and recently extinct members of the crested penguin genus Eudyptes. The new species has a markedly more slender upper beak and mandible compared with other Eudyptes penguins. Our combined evidence approach reveals that deep bills evolved in both crested and stiff-tailed penguins (Pygoscelis) during the Pliocene. That deep bills arose so late in the greater than 60 million year evolutionary history of penguins suggests that dietary shifts may have occurred as wind-driven Pliocene upwelling radically restructured southern ocean ecosystems. Ancestral area reconstructions using BioGeoBEARS identify New Zealand as the most likely ancestral area for total-group penguins, crown penguins and crested penguins. Our analyses provide a timeframe for recruitment of crown penguins into the New Zealand avifauna, indicating this process began in the late Neogene and was completed via multiple waves of colonizing lineages.

First monk seal from the Southern Hemisphere rewrites the evolutionary history of true seals.

Living true seals (phocids) are the most widely dispersed semi-aquatic marine mammals, and comprise geographically separate northern (phocine) and southern (monachine) groups. Both are thought to have evolved in the North Atlantic, with only two monachine lineages-elephant seals and lobodontins-subsequently crossing the equator. The third and most basal monachine tribe, the monk seals, have hitherto been interpreted as exclusively northern and (sub)tropical throughout their entire history. Here, we describe a new species of extinct monk seal from the Pliocene of New Zealand, the first of its kind from the Southern Hemisphere, based on one of the best-preserved and richest samples of seal fossils worldwide. This unanticipated discovery reveals that all three monachine tribes once coexisted south of the equator, and forces a profound revision of their evolutionary history: rather than primarily diversifying in the North Atlantic, monachines largely evolved in the Southern Hemisphere, and from this southern cradle later reinvaded the north. Our results suggest that true seals crossed the equator over eight times in their history. Overall, they more than double the age of the north-south dichotomy characterizing living true seals and confirms a surprisingly recent major change in southern phocid diversity.

Ancient DNA of crested penguins: Testing for temporal genetic shifts in the world's most diverse penguin clade.

Human impacts have substantially reduced avian biodiversity in many parts of the world, particularly on isolated islands of the Pacific Ocean. The New Zealand archipelago, including its five subantarctic island groups, holds breeding grounds for a third of the world's penguin species, including several representatives of the diverse crested penguin genus Eudyptes. While this species-rich genus has been little studied genetically, recent population estimates indicate that several Eudyptes taxa are experiencing demographic declines. Although crested penguins are currently limited to southern regions of the New Zealand archipelago, prehistoric fossil and archaeological deposits suggest a wider distribution during prehistoric times, with breeding ranges perhaps extending to the North Island. Here, we analyse ancient, historic and modern DNA sequences to explore two hypotheses regarding the recent history of Eudyptes in New Zealand, testing for (1) human-driven extinction of Eudyptes lineages; and (2) reduced genetic diversity in surviving lineages. From 83 prehistoric bone samples, each tentatively identified as 'Eudyptes spp.', we genetically identified six prehistoric penguin taxa from mainland New Zealand, including one previously undescribed genetic lineage. Moreover, our Bayesian coalescent analyses indicated that, while the range of Fiordland crested penguin (E. pachyrhynchus) may have contracted markedly over the last millennium, genetic DNA diversity within this lineage has remained relatively constant. This result contrasts with human-driven biodiversity reductions previously detected in several New Zealand coastal vertebrate taxa.

Blind free-living kiwi offer a unique window into the ecology and evolution of vertebrate vision.

The first report of multiple, blind, wild birds in good health suggests vision is not necessary for the survival of kiwi.

Ancient DNA and morphometric analysis reveal extinction and replacement of New Zealand's unique black swans.

Prehistoric human impacts on megafaunal populations have dramatically reshaped ecosystems worldwide. However, the effects of human exploitation on smaller species, such as anatids (ducks, geese, and swans) are less clear. In this study we apply ancient DNA and osteological approaches to reassess the history of Australasia's iconic black swans (Cygnus atratus) including the palaeo-behaviour of prehistoric populations. Our study shows that at the time of human colonization, New Zealand housed a genetically, morphologically, and potentially ecologically distinct swan lineage (C. sumnerensis, Pouwa), divergent from modern (Australian) C. atratus Morphological analyses indicate C. sumnerensis exhibited classic signs of the 'island rule' effect, being larger, and likely flight-reduced compared to C. atratus Our research reveals sudden extinction and replacement events within this anatid species complex, coinciding with recent human colonization of New Zealand. This research highlights the role of anthropogenic processes in rapidly reshaping island ecosystems and raises new questions for avian conservation, ecosystem re-wilding, and de-extinction.

Speciation, range contraction and extinction in the endemic New Zealand King Shag complex.

New Zealand's endemic King Shag (Leucocarbo carunculatus) has occupied only a narrow portion of the northeastern South Island for at least the past 240years. However, pre-human Holocene fossil and archaeological remains have suggested a far more widespread distribution of the three Leucocarbo species (King, Otago, Foveaux) on mainland New Zealand at the time of Polynesian settlement in the late 13th Century CE. We use modern and ancient DNA, and morphometric and osteological analyses, of modern King Shags and Holocene fossil Leucocarbo remains to assess the pre-human distribution and taxonomic status of the King Shag on mainland New Zealand, and the resultant conservation implications. Our analyses show that the King Shag was formerly widespread around southern coasts of the North Island and the northern parts of the South Island but experienced population and lineage extinctions, and range contraction, probably after Polynesian arrival. This history parallels range contractions of other New Zealand seabirds. Conservation management of the King Shag should take into account this species narrow distribution and probable reduced genetic diversity. Moreover, combined genetic, morphometric and osteological analyses of prehistoric material from mainland New Zealand suggest that the now extinct northern New Zealand Leucocarbo populations comprised a unique lineage. Although these distinctive populations were previously assigned to the King Shag (based on morphological similarities and geographic proximity to modern Leucocarbo populations), we herein describe them as a new species, the Kohatu Shag (Leucocarbo septentrionalis). The extinction of this species further highlights the dramatic impacts Polynesians and introduced predators had on New Zealand's coastal and marine biodiversity. The prehistoric presence of at least four species of Leucocarbo shag on mainland NZ further highlights its status as a biodiversity hotspot for Phalacrocoracidae.

Human-mediated extirpation of the unique Chatham Islands sea lion and implications for the conservation management of remaining New Zealand sea lion populations.

While terrestrial megafaunal extinctions have been well characterized worldwide, our understanding of declines in marine megafauna remains limited. Here, we use ancient DNA analyses of prehistoric (<1450-1650 AD) sea lion specimens from New Zealand's isolated Chatham Islands to assess the demographic impacts of human settlement. These data suggest there was a large population of sea lions, unique to the Chatham Islands, at the time of Polynesian settlement. This distinct mitochondrial lineage became rapidly extinct within 200 years due to overhunting, paralleling the extirpation of a similarly large endemic mainland population. Whole mitogenomic analyses confirm substantial intraspecific diversity among prehistoric lineages. Demographic models suggest that even low harvest rates would likely have driven rapid extinction of these lineages. This study indicates that surviving Phocarctos populations are remnants of a once diverse and widespread sea lion assemblage, highlighting dramatic human impacts on endemic marine biodiversity. Our findings also suggest that Phocarctos bycatch in commercial fisheries may contribute to the ongoing population decline.

Geographically contrasting biodiversity reductions in a widespread New Zealand seabird.

Unravelling prehistoric anthropogenic impacts on biodiversity represents a key challenge for biologists and archaeologists. New Zealand's endemic Stewart Island Shag (Leucocarbo chalconotus) comprises two distinct phylogeographic lineages, currently restricted to the country's south and southeast. However, fossil and archaeological remains suggest a far more widespread distribution at the time of Polynesian settlement ca. 1280 AD, encompassing much of coastal South Island. We used modern and ancient DNA, radiocarbon dating, and Bayesian modelling, to assess the impacts of human arrival on this taxon. Our analyses show that the southeast South Island (Otago) lineage was formerly widespread across coastal South Island, but experienced dramatic population extinctions, range retraction and lineage loss soon after human arrival. By comparison, the southernmost (Foveaux Strait) lineage has experienced a relatively stable demographic and biogeographic history since human arrival, retaining much of its mitochondrial diversity. Archaeological data suggest that these contrasting demographic histories (retraction vs. stability) reflect differential human impacts in mainland South Island vs. Foveaux Strait, highlighting the importance of testing for temporal and spatial variation in human-driven faunal declines.

Genomic analyses of fairy and fulmar prions (Procellariidae: Pachyptila spp.) reveals parallel evolution of bill morphology, and multiple species.

Prions are small petrels that are abundant around the Southern Ocean. Here we use mitochondrial DNA (COI and cytochrome b) and nuclear reduced representation sequencing (ddRADseq) to examine the relationships within and between fairy (Pachyptila turtur) and fulmar (P. crassirostris) prions from across their distributions. We found that neither species was recovered as monophyletic, and that at least three species were represented. Furthermore, we detected several genetic lineages that are also morphologically distinct occurring in near sympatry at two locations (Snares Islands and Chatham Islands). The factors that have driven diversification in the fairy/fulmar prion complex are unclear but may include philopatry, differences in foraging distribution during breeding, differences in non-breeding distributions and breeding habitat characteristics. The observed distribution of genetic variation in the fairy/fulmar prion complex is consistent with population expansion from ice-free Last Glacial Maximum refugia into previously glaciated areas.

Genomic insights into the secondary aquatic transition of penguins.

Penguins lost the ability to fly more than 60 million years ago, subsequently evolving a hyper-specialized marine body plan. Within the framework of a genome-scale, fossil-inclusive phylogeny, we identify key geological events that shaped penguin diversification and genomic signatures consistent with widespread refugia/recolonization during major climate oscillations. We further identify a suite of genes potentially underpinning adaptations related to thermoregulation, oxygenation, diving, vision, diet, immunity and body size, which might have facilitated their remarkable secondary transition to an aquatic ecology. Our analyses indicate that penguins and their sister group (Procellariiformes) have the lowest evolutionary rates yet detected in birds. Together, these findings help improve our understanding of how penguins have transitioned to the marine environment, successfully colonizing some of the most extreme environments on Earth.

Bats that walk: a new evolutionary hypothesis for the terrestrial behaviour of New Zealand's endemic mystacinids.

BACKGROUND: New Zealand's lesser short-tailed bat Mystacina tuberculata is one of only two of c.1100 extant bat species to use a true walking gait when manoeuvring on the ground (the other being the American common vampire bat Desmodus rotundus). Mystacina tuberculata is also the last surviving member of Mystacinidae, the only mammalian family endemic to New Zealand (NZ) and a member of the Gondwanan bat superfamily Noctilionoidea. The capacity for true quadrupedal terrestrial locomotion in Mystacina is a secondarily derived condition, reflected in numerous skeletal and muscular specializations absent in other extant bats. The lack of ground-based predatory native NZ mammals has been assumed to have facilitated the evolution of terrestrial locomotion and the unique burrowing behaviour of Mystacina, just as flightlessness has arisen independently many times in island birds. New postcranial remains of an early Miocene mystacinid from continental Australia, Icarops aenae, offer an opportunity to test this hypothesis. RESULTS: Several distinctive derived features of the distal humerus are shared by the extant Mystacina tuberculata and the early Miocene Australian mystacinid Icarops aenae. Study of the myology of M. tuberculata indicates that these features are functionally correlated with terrestrial locomotion in this bat. Their presence in I. aenae suggests that this extinct mystacinid was also adapted for terrestrial locomotion, despite the existence of numerous ground-based mammalian predators in Australia during the early Miocene. Thus, it appears that mystacinids were already terrestrially-adapted prior to their isolation in NZ. In combination with recent molecular divergence dates, the new postcranial material of I. aenae constrains the timing of the evolution of terrestrial locomotion in mystacinids to between 51 and 26 million years ago (Ma). CONCLUSION: Contrary to existing hypotheses, our data suggest that bats are not overwhelmingly absent from the ground because of competition from, or predation by, other mammals. Rather, selective advantage appears to be the primary evolutionary driving force behind habitual terrestriality in the rare bats that walk. Unlike for birds, there is currently no evidence that any bat has evolved a reduced capacity for flight as a result of isolation on islands.

A sphenodontine (Rhynchocephalia) from the Miocene of New Zealand and palaeobiogeography of the tuatara (Sphenodon).

Jaws and dentition closely resembling those of the extant tuatara (Sphenodon) are described from the Manuherikia Group (Early Miocene; 19-16 million years ago, Mya) of Central Otago, New Zealand. This material is significant in bridging a gap of nearly 70 million years in the rhynchocephalian fossil record between the Late Pleistocene of New Zealand and the Late Cretaceous of Argentina. It provides the first pre-Pleistocene record of Rhynchocephalia in New Zealand, a finding consistent with the view that the ancestors of Sphenodon have been on the landmass since it separated from the rest of Gondwana 82-60 Mya. However, if New Zealand was completely submerged near the Oligo-Miocene boundary (25-22 Mya), as recently suggested, an ancestral sphenodontine would need to have colonized the re-emergent landmass via ocean rafting from a currently unrecorded and now extinct Miocene population. Although an Early Miocene record does not preclude that possibility, it substantially reduces the temporal window of opportunity. Irrespective of pre-Miocene biogeographic history, this material also provides the first direct evidence that the ancestors of the tuatara, an animal often perceived as unsophisticated, survived in New Zealand despite substantial local climatic and environmental changes.

Miocene skinks and geckos reveal long-term conservatism of New Zealand's lizard fauna.

The New Zealand (NZ) lizard fossil record is currently limited to late Quaternary remains of modern taxa. The St Bathans Fauna (early Miocene, southern South Island) extends this record to 19-16 million years ago (Myr ago). Skull and postcranial elements are similar to extant Oligosoma (Lygosominae) skinks and Hoplodactylus (Diplodactylinae) geckos. There is no evidence of other squamate groups. These fossils, along with coeval sphenodontines, demonstrate a long conservative history for the NZ lepidosaurian fauna, provide new molecular clock calibrations and contradict inferences of a very recent (less than 8 Myr ago) arrival of skinks in NZ.

High-coverage genomes to elucidate the evolution of penguins.

BACKGROUND: Penguins (Sphenisciformes) are a remarkable order of flightless wing-propelled diving seabirds distributed widely across the southern hemisphere. They share a volant common ancestor with Procellariiformes close to the Cretaceous-Paleogene boundary (66 million years ago) and subsequently lost the ability to fly but enhanced their diving capabilities. With ∼20 species among 6 genera, penguins range from the tropical Galápagos Islands to the oceanic temperate forests of New Zealand, the rocky coastlines of the sub-Antarctic islands, and the sea ice around Antarctica. To inhabit such diverse and extreme environments, penguins evolved many physiological and morphological adaptations. However, they are also highly sensitive to climate change. Therefore, penguins provide an exciting target system for understanding the evolutionary processes of speciation, adaptation, and demography. Genomic data are an emerging resource for addressing questions about such processes. RESULTS: Here we present a novel dataset of 19 high-coverage genomes that, together with 2 previously published genomes, encompass all extant penguin species. We also present a well-supported phylogeny to clarify the relationships among penguins. In contrast to recent studies, our results demonstrate that the genus Aptenodytes is basal and sister to all other extant penguin genera, providing intriguing new insights into the adaptation of penguins to Antarctica. As such, our dataset provides a novel resource for understanding the evolutionary history of penguins as a clade, as well as the fine-scale relationships of individual penguin lineages. Against this background, we introduce a major consortium of international scientists dedicated to studying these genomes. Moreover, we highlight emerging issues regarding ensuring legal and respectful indigenous consultation, particularly for genomic data originating from New Zealand Taonga species. CONCLUSIONS: We believe that our dataset and project will be important for understanding evolution, increasing cultural heritage and guiding the conservation of this iconic southern hemisphere species assemblage.