​Comparative genomics of Balto, a famous historic dog, captures lost diversity of 1920s sled dogs.

We reconstruct the phenotype of Balto, the heroic sled dog renowned for transporting diphtheria antitoxin to Nome, Alaska, in 1925, using evolutionary constraint estimates from the Zoonomia alignment of 240 mammals and 682 genomes from dogs and wolves of the 21st century. Balto shares just part of his diverse ancestry with the eponymous Siberian husky breed. Balto's genotype predicts a combination of coat features atypical for modern sled dog breeds, and a slightly smaller stature. He had enhanced starch digestion compared with Greenland sled dogs and a compendium of derived homozygous coding variants at constrained positions in genes connected to bone and skin development. We propose that Balto's population of origin, which was less inbred and genetically healthier than that of modern breeds, was adapted to the extreme environment of 1920s Alaska.

Fifty million years of beetle evolution along the Antarctic Polar Front.

Global cooling and glacial-interglacial cycles since Antarctica's isolation have been responsible for the diversification of the region's marine fauna. By contrast, these same Earth system processes are thought to have played little role terrestrially, other than driving widespread extinctions. Here, we show that on islands along the Antarctic Polar Front, paleoclimatic processes have been key to diversification of one of the world's most geographically isolated and unique groups of herbivorous beetles-Ectemnorhinini weevils. Combining phylogenomic, phylogenetic, and phylogeographic approaches, we demonstrate that these weevils colonized the sub-Antarctic islands from Africa at least 50 Ma ago and repeatedly dispersed among them. As the climate cooled from the mid-Miocene, diversification of the beetles accelerated, resulting in two species-rich clades. One of these clades specialized to feed on cryptogams, typical of the polar habitats that came to prevail under Miocene conditions yet remarkable as a food source for any beetle. This clade's most unusual representative is a marine weevil currently undergoing further speciation. The other clade retained the more common weevil habit of feeding on angiosperms, which likely survived glaciation in isolated refugia. Diversification of Ectemnorhinini weevils occurred in synchrony with many other Antarctic radiations, including penguins and notothenioid fishes, and coincided with major environmental changes. Our results thus indicate that geo-climatically driven diversification has progressed similarly for Antarctic marine and terrestrial organisms since the Miocene, potentially constituting a general biodiversity paradigm that should be sought broadly for the region's taxa.

Environmental genomics of Late Pleistocene black bears and giant short-faced bears.

Analysis of ancient environmental DNA (eDNA) has revolutionized our ability to describe biological communities in space and time,1-3 by allowing for parallel sequencing of DNA from all trophic levels.4-8 However, because environmental samples contain sparse and fragmented data from multiple individuals, and often contain closely related species,9 the field of ancient eDNA has so far been limited to organellar genomes in its contribution to population and phylogenetic studies.5,6,10,11 This is in contrast to data from fossils12,13 where full-genome studies are routine, despite these being rare and their destruction for sequencing undesirable.14-16 Here, we report the retrieval of three low-coverage (0.03×) environmental genomes from American black bear (Ursus americanus) and a 0.04× environmental genome of the extinct giant short-faced bear (Arctodus simus) from cave sediment samples from northern Mexico dated to 16-14 thousand calibrated years before present (cal kyr BP), which we contextualize with a new high-coverage (26×) and two lower-coverage giant short-faced bear genomes obtained from fossils recovered from Yukon Territory, Canada, which date to ∼22-50 cal kyr BP. We show that the Late Pleistocene black bear population in Mexico is ancestrally related to the present-day Eastern American black bear population, and that the extinct giant short-faced bears present in Mexico were deeply divergent from the earlier Beringian population. Our findings demonstrate the ability to separately analyze genomic-scale DNA sequences of closely related species co-preserved in environmental samples, which brings the use of ancient eDNA into the era of population genomics and phylogenetics.

Springtail phylogeography highlights biosecurity risks of repeated invasions and intraregional transfers among remote islands.

Human-mediated transport of species outside their natural range is a rapidly growing threat to biodiversity, particularly for island ecosystems that have evolved in isolation. The genetic structure underpinning island populations will largely determine their response to increased transport and thus help to inform biosecurity management. However, this information is severely lacking for some groups, such as the soil fauna. We therefore analysed the phylogeographic structure of an indigenous and an invasive springtail species (Collembola: Poduromorpha), each distributed across multiple remote sub-Antarctic islands, where human activity is currently intensifying. For both species, we generated a genome-wide SNP data set and additionally analysed all available COI barcodes. Genetic differentiation in the indigenous springtail Tullbergia bisetosa is substantial among (and, to a lesser degree, within) islands, reflecting low dispersal and historic population fragmentation, while COI patterns reveal ancestral signatures of postglacial recolonization. This pronounced geographic structure demonstrates the key role of allopatric divergence in shaping the region's diversity and highlights the vulnerability of indigenous populations to genetic homogenization via human transport. For the invasive species Hypogastrura viatica, nuclear genetic structure is much less apparent, particularly for islands linked by regular shipping, while diverged COI haplotypes indicate multiple independent introductions to each island. Thus, human transport has likely facilitated this species' persistence since its initial colonization, through the ongoing introduction and inter-island spread of genetic variation. These findings highlight the different evolutionary consequences of human transport for indigenous and invasive soil species. Crucially, both outcomes demonstrate the need for improved intraregional biosecurity among remote island systems, where the policy focus to date has been on external introductions.

Can a Terrestrial Ectoparasite Disperse with Its Marine Host?

One of the most extreme examples of parasite adaptation comes from terrestrial ectoparasites exploiting marine hosts. Despite the ubiquity of such ectoparasitism and its ecological and evolutionary importance, investigations of the responses of ectoparasites to conditions encountered on their hosts are rare. In the case of penguins and their ticks, current understanding suggests that ticks freely parasitize their hosts on land but are incapable of surviving extended oceanic journeys. We examined this conjecture by assessing the physiological capacity of little penguin ticks to endure at-sea foraging and dispersal events of their hosts. Survival in penguins ticks was not significantly compromised by exposure to depths commonly associated with host dives (40 and 60 m), repeated seawater exposure relevant to the most common (30 s) and longest (120 s) recorded host dives, or extended (48 h) exposure to seawater. Mean (±SD) closed-phase durations in adult and nymphal ticks exhibiting discontinuous gas exchange ( 339±237 and 240±295 s, respectively) exceeded that of the maximum recorded host dive duration (120 s). Normoxic-anoxic-normoxic respirometry also confirmed spiracle closure. Mean metabolic rates ( 0.354±0.220 and 4.853±4.930 µL/h at 25°C for unfed and fed adult females, respectively) were significantly influenced by temperature; optimal and LT50 temperatures for adult ticks and fed nymphal ticks were typically higher than swimming penguin body temperatures. These findings suggest that marine host dispersal is unlikely to present an insurmountable barrier to long-distance tick dispersal. Such dispersal has important implications for evolutionary theory, conservation, and epidemiology.

Australian penguin ticks screened for novel Borrelia species.

Lyme borreliosis (or Lyme Disease) is an emerging threat to human health in the Northern Hemisphere caused by tick-borne bacteria from the Borrelia burgdorferi sensu lato (Bbsl) complex. Seabirds are important reservoir hosts of some members of the Bbsl complex in the Northern Hemisphere, and some evidence suggests this may be true of penguins in the Southern Hemisphere. While the Bbsl complex has not been detected in Australia, a novel Borrelia species ('Candidatus Borrelia tachyglossi') was recently sequenced from native ticks (Ixodes holocyclus and Bothriocroton concolor) parasitising echidnas (Tachyglossus aculeatus), suggesting unidentified borreliae may be circulating amongst native wildlife and their ticks. In the present study, we investigated whether ticks parasitising little penguins (Eudyptula novaehollandiae) harbour native or introduced Borrelia bacteria. We chose this penguin species because it is heavily exploited by ticks during the breeding season, lives in close proximity to other potential reservoir hosts (including native wildlife and migratory seabirds), and is known to be infected with other tick-borne pathogens (Babesia). We screened over 230 penguin ticks (Ixodes spp.) from colonies in south-eastern Australia, and found no evidence of Borrelia DNA. The apparent absence or rarity of the bacterium in south-eastern Australia has important implications for identifying potential tick-borne pathogens in an understudied region.

Reconsidering connectivity in the sub-Antarctic.

Extreme and remote environments provide useful settings to test ideas about the ecological and evolutionary drivers of biological diversity. In the sub-Antarctic, isolation by geographic, geological and glaciological processes has long been thought to underpin patterns in the region's terrestrial and marine diversity. Molecular studies using increasingly high-resolution data are, however, challenging this perspective, demonstrating that many taxa disperse among distant sub-Antarctic landmasses. Here, we reconsider connectivity in the sub-Antarctic region, identifying which taxa are relatively isolated, which are well connected, and the scales across which this connectivity occurs in both terrestrial and marine systems. Although many organisms show evidence of occasional long-distance, trans-oceanic dispersal, these events are often insufficient to maintain gene flow across the region. Species that do show evidence of connectivity across large distances include both active dispersers and more sedentary species. Overall, connectivity patterns in the sub-Antarctic at intra- and inter-island scales are highly complex, influenced by life-history traits and local dynamics such as relative dispersal capacity and propagule pressure, natal philopatry, feeding associations, the extent of human exploitation, past climate cycles, contemporary climate, and physical barriers to movement. An increasing use of molecular data - particularly genomic data sets that can reveal fine-scale patterns - and more effective international collaboration and communication that facilitates integration of data from across the sub-Antarctic, are providing fresh insights into the processes driving patterns of diversity in the region. These insights offer a platform for assessing the ways in which changing dispersal mechanisms, such as through increasing human activity and changes to wind and ocean circulation, may alter sub-Antarctic biodiversity patterns in the future.

Phylogeographic Structure in Penguin Ticks across an Ocean Basin Indicates Allopatric Divergence and Rare Trans-Oceanic Dispersal.

The association of ticks (Acarina) and seabirds provides an intriguing system for assessing the influence of long-distance dispersal on the evolution of parasitic species. Recent research has focused on host-parasite evolutionary relationships and dispersal capacity of ticks parasitising flighted seabirds. Evolutionary research on the ticks of non-flighted seabirds is, in contrast, scarce. We conducted the first phylogeographic investigation of a hard tick species (Ixodes eudyptidis) that parasitises the Little Blue Penguin (Eudyptula minor). Using one nuclear (28S) and two mitochondrial (COI and 16S) markers, we assessed genetic diversity among several populations in Australia and a single population on the South Island of New Zealand. Our results reveal two deeply divergent lineages, possibly representing different species: one comprising all New Zealand samples and some from Australia, and the other representing all other samples from Australian sites. No significant population differentiation was observed among any Australian sites from within each major clade, even those separated by hundreds of kilometres of coastline. In contrast, the New Zealand population was significantly different to all samples from Australia. Our phylogenetic results suggest that the New Zealand and Australian populations are effectively isolated from each other; although rare long-distance dispersal events must occur, these are insufficient to maintain trans-Tasman gene flow. Despite the evidence for limited dispersal of penguin ticks between Australia and New Zealand, we found no evidence to suggest that ticks are unable to disperse shorter distances at sea with their hosts, with no pattern of population differentiation found among Australian sites. Our results suggest that terrestrial seabird parasites may be quite capable of short-distance movements, but only sporadic longer-distance (trans-oceanic) dispersal.

The changing form of Antarctic biodiversity.

Antarctic biodiversity is much more extensive, ecologically diverse and biogeographically structured than previously thought. Understanding of how this diversity is distributed in marine and terrestrial systems, the mechanisms underlying its spatial variation, and the significance of the microbiota is growing rapidly. Broadly recognizable drivers of diversity variation include energy availability and historical refugia. The impacts of local human activities and global environmental change nonetheless pose challenges to the current and future understanding of Antarctic biodiversity. Life in the Antarctic and the Southern Ocean is surprisingly rich, and as much at risk from environmental change as it is elsewhere.