Invader or resident? Ancient-DNA reveals rapid species turnover in New Zealand little penguins

The expansion of humans into previously unoccupied parts of the globe is thought to have driven the decline and extinction of numerous vertebrate species. In New Zealand, human settlement in the late thirteenth century AD led to the rapid demise of a distinctive vertebrate fauna, and also a number of ''turnover'' events where extinct lineages were subsequently replaced by closely related taxa. The recent genetic detection of an Australian little penguin (Eudyptula novaehollandiae) in southeastern New Zealand may potentially represent an additional ‘cryptic’ invasion. Here we use ancient-DNA (aDNA) analysis and radiocarbon dating of pre-human, archaeological and historical Eudyptula remains to reveal that the arrival of E. novaehollandiae in New Zealand probably occurred between AD 1500 and 1900, following the anthropogenic decline of its sister taxon, the endemic Eudyptula minor. This rapid turnover event, revealed by aDNA, suggests that native species decline can be masked by invasive taxa, and highlights the potential for human-mediated biodiversity shifts.     

Evidence for breeding of Megadyptes penguins in the North Island at the time of human arrival

The arrival of humans in New Zealand around 750 years ago resulted in widespread faunal extinctions including the endemic Waitaha penguin (Megadyptes waitaha). Previously thought to have only bred on coastal South Island and Stewart Island, recent genetic reanalysis of prehistoric large penguin bones from the lower North Island indicates that the Waitaha penguin may have been a common resident. Here we synthesise previous studies and present new palaeontological and archaeological evidence to suggest that the Waitaha penguin was probably breeding in the lower North Island at the time of human arrival, and did not represent vagrant individuals from more southerly breeding colonies. The elimination of breeding Megadyptes from the North Island would add to the already significant avifaunal losses from New Zealand, of which the North Island suffered the greatest biodiversity loss after the arrival of humans.     

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.     

Phylogeny of the Bangia flora of New Zealand suggests a southern origin for Porphyra and Bangia (Bangiales, Rhodophyta)

Analysis of nuclear small subunit ribosomal RNA gene (18S rDNA) sequence data from 123 samples of the red algal genus Bangia from mainland New Zealand has revealed diversity exceeding that reported for the genus from any other region in the world. Our study resolves two New Zealand Bangia taxa basal to the order Bangiales, and five clades of Bangia, four of which include New Zealand members. The basal taxa are separated from each other by 139 bp and differ from all other Bangia taxa in the New Zealand region by 103-163 bp over approximately 1750 bp 18S rDNA sequence data. Our results reveal a Bangia flora of previously unsuspected richness, and show that the simple morphology of these organisms obscures significant levels of genetic diversity. The presence of high diversity and retention of basal taxa in New Zealand Bangia raises the prospect that the southern hemisphere, and particularly eastern Gondwana, is not only a centre of diversity, but a centre of origin for the modern Bangiales.     

Crossing the Tasman Sea: Inferring the introduction history of Litoria aurea and Litoria raniformis (Anura: Hylidae) from Australia into New Zealand

Abstract The amphibian fauna of New Zealand consists of three native species (Leiopelma spp.), and three Litoria species introduced from Australia in the last 140 years. We conducted a molecular phylogeographical study that aimed to identify the Australian origins of two species, Litoria aurea and Litoria raniformis. We used partial sequences of the mitochondrial cytochrome oxidase I (cox1) gene from 59 specimens sampled from across the range of both species to identify the probable source populations for the New Zealand introductions, and to describe the current genetic diversity among New Zealand Litoria populations. Our genetic data suggest that L. aurea was introduced into the North Island of New Zealand from two regions in Australia, once from the northern part of coastal New South Wales and once from the southern part of coastal New South Wales. Our data indicate that L. raniformis introductions originated from the Melbourne region of southern Victoria and once established in the South Island of New Zealand, the species subsequently spread throughout both islands. In addition, we found a distinct haplotype in L. raniformis from Tasmania that strongly suggests, contrary to earlier reports, that this species was not introduced into New Zealand from Tasmania. Finally, we identified two very distinctive mitochondrial lineages of L. raniformis within the mainland Australia distribution, which may be previously unrecognized species.     

Ancient DNA Resolves Identity and Phylogeny of New Zealand's Extinct and Living Quail (Coturnix sp.)

Background

The New Zealand quail, Coturnix novaezealandiae, was widespread throughout New Zealand until its rapid extinction in the 1870''s. To date, confusion continues to exist concerning the identity of C. novaezealandiae and its phylogenetic relationship to Coturnix species in neighbouring Australia, two of which, C. ypsilophora and C. pectoralis, were introduced into New Zealand as game birds. The Australian brown quail, C. ypsilophora, was the only species thought to establish with current populations distributed mainly in the northern part of the North Island of New Zealand. Owing to the similarities between C. ypsilophora, C. pectoralis, and C. novaezealandiae, uncertainty has arisen over whether the New Zealand quail is indeed extinct, with suggestions that remnant populations of C. novaezealandiae may have survived on offshore islands.

Methodology/Principal Findings

Using fresh and historical samples of Coturnix sp. from New Zealand and Australia, DNA analysis of selected mitochondrial regions was carried out to determine phylogenetic relationships and species status. Results show that Coturnix sp. specimens from the New Zealand mainland and offshore island Tiritiri Matangi are not the New Zealand quail but are genetically identical to C. ypsilophora from Australia and can be classified as the same species. Furthermore, cytochrome b and COI barcoding analysis of the New Zealand quail and Australia''s C. pectoralis, often confused in museum collections, show that they are indeed separate species that diverged approximately 5 million years ago (mya). Gross morphological analysis of these birds suggests a parallel loss of sustained flight with very little change in other phenotypic characters such as plumage or skeletal structure.

Conclusion/Significance

Ancient DNA has proved invaluable for the detailed analysis and identification of extinct and morphologically cryptic taxa such as that of quail and can provide insights into the timing of evolutionary changes that influence morphology.     

Gastrointestinal helminths of little blue penguins,Eudyptula novaehollandiae (Stephens), from Otago,New Zealand

Data regarding helminth communities can provide insights into health, feeding interactions, behaviour and evolution of their host organisms. Penguins (Spheniscidae) are important components of marine food webs and tracking their helminth communities can be indicative of ecosystem health. New Zealand is home to 5 of the world's 19 penguin species and little is known about their gastrointestinal helminths. Here, we provide the first study on the gastrointestinal helminths of little blue penguins from south-eastern South Island, New Zealand. The helminth community consisted of two species of tapeworm; Tetrabothrius lutzi and Tetrabothrius sp.; three nematode species, Contracaecum eudyptulae, Capillaria sp. and Stegophorus macronectes; two acanthocephalans, Andracantha sigma and Bolbosoma balaenae; and one trematode, Galactosomum otepotiense. The most prevalent parasites were T. lutzi, A. sigma, and C. eudyptulae. This work includes three new host records and five new geographic records. This is the first report of B. balaenae occurring in a host other than a marine mammal. This study adds to our knowledge about the helminth community of New Zealand little blue penguins, and includes new genetic data on helminth species, providing a baseline against which future studies may be compared.     

The phylogeny of the living and fossil Sphenisciformes (penguins)

We present the first phylogenetic analysis of the Sphenisciformes that extensively samples fossil taxa. Combined analysis of 181 morphological characters and sequence fragments from mitochondrial and nuclear genes (12S, 16S, COI, cytochrome b, RAG‐1) yields a largely resolved tree. Two species of the New Zealand Waimanu form a trichotomy with all other penguins in our result. The much discussed giant penguins Anthropornis and Pachydyptes are placed in two clades near the base of the tree. Stratigraphic and phylogenetic evidence suggest that some lineages of penguins attained very large body size rapidly and early in the clade's evolutionary history. The only fossil taxa that fall inside the crown clade Spheniscidae are fossil species assigned to the genus Spheniscus. Thus, extant penguin diversity is more accurately viewed as the product of a successful radiation of derived taxa than as an assemblage of survivors belonging to numerous lineages. The success of the Spheniscidae may be due to novel feeding adaptations and a more derived flipper apparatus. We offer a biogeographical scenario for penguins that incorporates fossil distributions and paleogeographic reconstructions of the Southern continent's positions. Our results do not support an expansion of the Spheniscidae from a cooling Continental Antarctica, but instead suggest those species that currently breed in that area are the descendants of colonizers from the Subantarctic. Many important divergence events in the clade Spheniscidae can instead be explained by dispersal along the paths of major ocean currents and the emergence of new islands due to tectonic events. © The Willi Hennig Society 2006.     

Marine Biodiversity of Aotearoa New Zealand

The marine-biodiversity assessment of New Zealand (Aotearoa as known to Māori) is confined to the 200 nautical-mile boundary of the Exclusive Economic Zone, which, at 4.2 million km², is one of the largest in the world. It spans 30° of latitude and includes a high diversity of seafloor relief, including a trench 10 km deep. Much of this region remains unexplored biologically, especially the 50% of the EEZ deeper than 2,000 m. Knowledge of the marine biota is based on more than 200 years of marine exploration in the region. The major oceanographic data repository is the National Institute of Water and Atmospheric Research (NIWA), which is involved in several Census of Marine Life field projects and is the location of the Southwestern Pacific Regional OBIS Node; NIWA is also data manager and custodian for fisheries research data owned by the Ministry of Fisheries. Related data sources cover alien species, environmental measures, and historical information. Museum collections in New Zealand hold more than 800,000 registered lots representing several million specimens. During the past decade, 220 taxonomic specialists (85 marine) from 18 countries have been engaged in a project to review New Zealand''s entire biodiversity. The above-mentioned marine information sources, published literature, and reports were scrutinized to give the results summarized here for the first time (current to 2010), including data on endemism and invasive species. There are 17,135 living species in the EEZ. This diversity includes 4,315 known undescribed species in collections. Species diversity for the most intensively studied phylum-level taxa (Porifera, Cnidaria, Mollusca, Brachiopoda, Bryozoa, Kinorhyncha, Echinodermata, Chordata) is more or less equivalent to that in the ERMS (European Register of Marine Species) region, which is 5.5 times larger in area than the New Zealand EEZ. The implication is that, when all other New Zealand phyla are equally well studied, total marine diversity in the EEZ may be expected to equal that in the ERMS region. This equivalence invites testable hypotheses to explain it. There are 177 naturalized alien species in New Zealand coastal waters, mostly in ports and harbours. Marine-taxonomic expertise in New Zealand covers a broad number of taxa but is, proportionately, at or near its lowest level since the Second World War. Nevertheless, collections are well supported by funding and are continually added to. Threats and protection measures concerning New Zealand''s marine biodiversity are commented on, along with potential and priorities for future research.     

History, current status and future of marine macroalgal research in New Zealand: Taxonomy, ecology, physiology and human uses

New Zealand has a rich and diverse macroalgal flora that has been studied since James Cook's first voyage to New Zealand in 1769. The New Zealand region ranges from cool temperate seas at southerly latitudes to subtropical waters in the north. Here we review the history of phycological research in New Zealand since 1900, and the current status of research in taxonomy, ecology, physiology and seaweed uses including aqua‐culture and seaweed extracts. Some 770 species of seaweed are known to New Zealand, of which 22 are alien. Few taxa have received monographic treatment and many remain to be described. Polysaccharides have been identified from over 80 New Zealand seaweeds and many of these compounds have commercial potential. In addition to urgent taxonomic work, future research should include a national program of long‐term (> 5 years) monitoring of macroalgal communities, rates of growth and primary production, and the contribution of seaweed‐based production to coastal food webs.     

Genetic divergence between isolated populations of the North Island New Zealand Rifleman (Acanthisitta chloris granti) implicates ancient biogeographic impacts rather than recent habitat fragmentation

This research investigates the extent and causal mechanisms of genetic population divergence in a poorly flighted passerine, the North Island Rifleman or Titipounamu (Acanthisitta chloris granti). While this species has a historically widespread distribution, anthropogenic forest clearance has resulted in a highly fragmented current distribution. We conducted analyses of mitochondrial DNA (COI and Control Region) and 12 nuclear DNA microsatellites to test for population divergence and estimate times of divergence. diyabc and biogeobears were then used to assess likely past dispersal scenarios based on both mtDNA and nDNA. The results reveal several significantly divergent lineages across the North Island of New Zealand and indicate that some populations have been isolated for extensive periods of time (0.7–4.9 mya). Modeling indicated a dynamic history of population connectivity, with a drastic restriction in gene flow between three geographic regions, followed by a more recent re‐establishment of connectivity. Our analyses indicate the dynamic influence of key geological and climatological events on the distribution of genetic diversity in this species, including support for the genetic impact of old biogeographic boundaries such as the Taupo Line and Cockayne''s Line, rather than recent anthropogenic habitat fragmentation. These findings present a rare example of an avian species with a genetic history more like that of flightless taxa and so provide new general insights into vicariant processes affecting populations of passerines with limited dispersal.     

The genetic architecture of hybridisation between two lineages of greenshell mussels

A multidisciplinary approach has identified sigmoidal genetic clines on the east and west coasts in central New Zealand where low-density ecological interactions occur between northern and southern lineages of the endemic greenshell mussel, Perna canaliculus. The sigmoidal clines indicate the existence of a mussel hybrid zone in a region of genetic discontinuities for many continuously distributed coastal taxa, in particular marine invertebrates. Examination of the genetic architecture of the hybrid zone revealed the differential contribution of individual microsatellite loci and/or alleles to defining the zone of interaction and no evidence of increased allelic richness or heterozygosity inside versus outside the hybrid zone. Genomics cline analysis identified one locus in particular (Pcan1–27) as being different from neutral expectations, thereby contributing to lineage differentiation. Estimates of contemporary gene flow revealed very high levels of within-lineage self-recruitment and a hybrid zone composed mostly (~85%) of northern immigrants. Broad scale interpretation of these results is consistent with a zone of genetic interaction that was generated between 0.3 and 1.3 million years before present at a time of pronounced global sea-level change. At that time, the continuous distribution of the greenshell mussel was split into northern and southern groups, which differentiated to become distinct lineages, and which have subsequently been reunited (secondary contact) resulting in the generation of the hybrid zone at ~42°S.     

Phylogenetic Position and Subspecies Divergence of the Endangered New Zealand Dotterel (Charadrius obscurus)

The New Zealand Dotterel (Charadrius obscurus), an endangered shorebird of the family Charadriidae, is endemic to New Zealand where two subspecies are recognized. These subspecies are not only separated geographically, with C. o. aquilonius being distributed in the New Zealand North Island and C. o. obscurus mostly restricted to Stewart Island, but also differ substantially in morphology and behavior. Despite these divergent traits, previous work has failed to detect genetic differentiation between the subspecies, and the question of when and where the two populations separated is still open. Here, we use mitochondrial and nuclear markers to address molecular divergence between the subspecies, and apply maximum likelihood and Bayesian methods to place C. obscurus within the non-monophyletic genus Charadrius. Despite very little overall differentiation, distinct haplotypes for the subspecies were detected, thus supporting molecular separation of the northern and southern populations. Phylogenetic analysis recovers a monophyletic clade combining the New Zealand Dotterel with two other New Zealand endemic shorebirds, the Wrybill and the Double-Banded Plover, thus suggesting a single dispersal event as the origin of this group. Divergence dates within Charadriidae were estimated with BEAST 2, and our results indicate a Middle Miocene origin of New Zealand endemic Charadriidae, a Late Miocene emergence of the lineage leading to the New Zealand Dotterel, and a Middle to Late Pleistocene divergence of the two New Zealand Dotterel subspecies.     

Population genetic structure and taxonomy of the common dolphin (Delphinus sp.) at its southernmost range limit: New Zealand waters

New Zealand is the southernmost limit of the common dolphin's (genus Delphinus) distribution in the Pacific Ocean. In this area, common dolphins occur in both coastal and oceanic habitats, exhibit seasonal and resident occurrence, and present high morphological variability. Here we investigated the population structure and the taxonomic identity of common dolphins (Delphinus sp.) within New Zealand waters using 14 microsatellite loci, 577 bp of the mtDNA control region, and 1,120 bp of the mtDNA cytochrome b gene across 90 individuals. We found high genetic variability and evidence of population expansion. Phylogenetic analyses conducted to clarify the taxonomic status of New Zealand common dolphins did not show any clustering reflecting geographic origin or morphotypes. The microsatellite analysis showed genetic differentiation between Coastal and Oceanic putative populations, while mtDNA revealed significant genetic differentiation only between the Hauraki Gulf and other putative groups. Our results suggest that differences in habitat choice and possible female site fidelity may play a role in shaping population structure of New Zealand common dolphins.     

Tracing the Tiger: Population Genetics Provides Valuable Insights into the Aedes (Stegomyia) albopictus Invasion of the Australasian Region

Background

The range of the Asian tiger mosquito Aedes albopictus is expanding globally, raising the threat of emerging and re-emerging arbovirus transmission risks including dengue and chikungunya. Its detection in Papua New Guinea''s (PNG) southern Fly River coastal region in 1988 and 1992 placed it 150 km from mainland Australia. However, it was not until 12 years later that it appeared on the Torres Strait Islands. We hypothesized that the extant PNG population expanded into the Torres Straits as an indirect effect of drought-proofing the southern Fly River coastal villages in response to El Nino-driven climate variability in the region (via the rollout of rainwater tanks and water storage containers).

Methodology/Principal Findings

Examination of the mosquito''s mitochondrial DNA cytochrome oxidase I (COI) sequences and 13 novel nuclear microsatellites revealed evidence of substantial intermixing between PNG''s southern Fly region and Torres Strait Island populations essentially compromising any island eradication attempts due to potential of reintroduction. However, two genetically distinct populations were identified in this region comprising the historically extant PNG populations and the exotic introduced population. Both COI sequence data and microsatellites showed the introduced population to have genetic affinities to populations from Timor Leste and Jakarta in the Indonesian region.

Conclusions/Significance

The Ae. albopictus invasion into the Australian region was not a range expansion out of PNG as suspected, but founded by other, genetically distinct population(s), with strong genetic affinities to populations sampled from the Indonesian region. We now suspect that the introduction of Ae. albopictus into the Australian region was driven by widespread illegal fishing activity originating from the Indonesian region during this period. Human sea traffic is apparently shuttling this mosquito between islands in the Torres Strait and the southern PNG mainland and this extensive movement may well compromise Ae. albopictus eradication attempts in this region.     

Observations on bipolar disjunctions of moonwort ferns (Botrychium,Ophioglossaceae)

Peter Raven, in 1963, included two fern taxa of the genus Botrychium in his list of plant species exhibiting American amphitropical bipolar disjunctions. He attributed the southern hemisphere occurrences to post‐Pleistocene long‐distance dispersal from counterparts in the northern hemisphere, probably assisted by annual bird migrations between the disjunct areas. Using genetic evidence gathered through worldwide analyses of phylogenetic relationship in Botrychium, we now review and reconsider Raven's conclusions. Genetic similarities indicate that South American Botrychium dusenii is an allotetraploid taxon closely related to B. spathulatum, a North American endemic, and that B. lunaria in New Zealand possesses a genotype identical to that of a taxon in North America derived through introgressive hybridization between B. lunaria and an endemic North American species, B. neolunaria. Both North American counterparts exhibit Raven's characteristics of bipolar disjuncts in their occurrence in mountain and coastal meadows, copious production of small propagules (spores in Botrychium), occurrence in habitats frequented by transpolar bird migrants, and ability to found new colonies through inbreeding. We discuss these characteristics in Botrychium and relative to other ferns and suggest further studies on Botrychium and related taxa to address questions of time, number, and mode of bipolar dispersals.     

Species Radiation of Carabid Beetles (Broscini: Mecodema) in New Zealand

New Zealand biodiversity has often been viewed as Gondwanan in origin and age, but it is increasingly apparent from molecular studies that diversification, and in many cases origination of lineages, postdate the break-up of Gondwanaland. Relatively few studies of New Zealand animal species radiations have as yet been reported, and here we consider the species-rich genus of carabid beetles, Mecodema. Constrained stratigraphic information (emergence of the Chatham Islands) and a substitution rate for Coleoptera were separately used to calibrate Bayesian relaxed molecular clock date estimates for diversification of Mecodema. The inferred timings indicate radiation of these beetles no earlier than the mid-Miocene with most divergences being younger, dating to the Plio-Pleistocene. A shallow age for the radiation along with a complex spatial distribution of these taxa involving many instances of sympatry implicates recent ecological speciation rather than a simplistic allopatric model. This emphasises the youthful and dynamic nature of New Zealand evolution that will be further elucidated with detailed ecological and population genetic analyses.     

Population structure and phylogeography of the short-tailed stingray, Dasyatis brevicaudata (Hutton 1875), in the Southern Hemisphere

There is accumulating evidence that the degree of vagility explains little of the extent of population subdivision found within elasmobranch species. Instead, patterns of gene flow in elasmobranchs appear more closely linked to the presence of dispersal barriers, either physical or biological. Here, we investigate the potential role of some of these isolating mechanisms in shaping the population structure of a member of the stingray family Dasyatidae (Dasyatis brevicaudata) at various scales (southern hemisphere vs. coastal New Zealand). Analyses of the mitochondrial DNA control region from 176 individuals revealed significant genetic structure between South Africa, Australia, and New Zealand populations (analysis of molecular variance [AMOVA], overall Ф(ST) = 0.67, P < 0.001), although New Zealand and Australia shared some haplotypes. Surprisingly, significant population differentiation was found among several coastal New Zealand locations (AMOVA, overall Ф(ST) = 0.05, P < 0.05). However, data did not support the genetic differentiation between individuals from an offshore breeding area and mainland individuals. Comparisons suggest that these stingrays exhibit similar levels of population differentiation as other coastal elasmobranchs, with high divergence across oceanic basins and lower differentiation along continuous coastal habitats. Differences in coastal population structuring in elasmobranch species studied to date may be attributed to species-specific preferences for coastal habitats, which may be linked to life history functions (e.g., feeding and pupping).     

Understanding sampling and taxonomic biases recorded by citizen scientists

Projects involving citizen scientists have greatly increased over the last decade and understanding errors associated with such projects has been identified as an important step. NatureWatch NZ is a biodiversity recording system accessible to members of the public. The “NZ wasps, ants, bees and parasitoids (Hymenoptera) project” was initiated within NatureWatch NZ in December 2012, and comparisons were analysed between these records and the known Hymenoptera fauna of the New Zealand region. Over the course of 1 year 25 members contributed 360 records from 186 taxa, including the discovery of several introduced species new to New Zealand. There was a strong geographical bias to the records, with the majority being based around the major cities. Aculeates (stinging wasps) were significantly over-represented in the NatureWatch records. Only half (55 %) of taxa were identified to species level, with a further 28 % at genus level, and 17 % identified above genus level (family, order). Furthermore, the majority (65 %) of taxa were recorded only once, and only a few taxa were recorded >5 times (top records were “Ichneumonidae”, “Hymenoptera”, Anthidium manicatum, and Apis mellifera). It is probable that these same biases also exist for many other taxonomic groups in projects operated by citizen scientists lacking set protocols. Caution should be exercised on the subsequent use, compilation, and analysis of citizen science, especially without prior examination of records and potential biases.