Michael Knapp’s research while affiliated with University of Otago and other places

In a changing environment, vacant niches can be filled either by adaptation of local taxa or range‐expanding invading species. The relative tempo of these patterns is of key interest in the modern age of climate change. Aotearoa New Zealand has been a hotspot of biogeographic research for decades due to its long‐term isolation and dramatic geological history. An island with high levels of faunal endemicity, it is a system well suited to studying the relative effects of in situ evolution versus dispersal in determining faunal assemblages, while its turbulent climate and geological history provide valuable insights into the evolutionary impacts of environmental changes. Such investigations are of urgent importance given predicted climate change and human impacts rapidly affecting environments globally. Here, we analyse the divergence dates of nearly all endemic Aotearoa New Zealand bird species from their overseas relatives to assess the role of environmental changes in driving speciation and colonisation, with special regard to cooling climate during the Pliocene and Pleistocene. We uncover a wave of colonisation events by Australian open‐habitat adapted species since the Pliocene that peaked at the beginning of the Pleistocene. Furthermore, we highlight an even distribution of divergence dates in forest‐adapted taxa through time, consistent with millions of years of extensive forest cover. Finally, we note parallels to the modern‐day establishment of new bird populations from Australia and suggest this is largely influenced by anthropogenic land‐use patterns. This research contributes to the growing body of work recognising the long‐lasting impacts of Pleistocene climate change on Aotearoa New Zealand's avifauna, and reinforces biological invasions as a key evolutionary response to changing environmental conditions.

Mitochondrial genomes (mitogenomes) represent a relatively cost-effective tool for comparing diversity between contemporary and historical populations to assess impacts of past population processes, or the outcomes of conservation management. The Aotearoa New Zealand endemic kakī| black stilt (Himantopus novaezelandiae) is a critically endangered wading bird. Anthropogenic impacts contributed to kakī declining to ~ 23 individuals in 1981 and promoted interspecific hybridisation with their more common congener, the poaka| pied stilt (H. leucocephalus). Conservation management of kakī has resulted in the population increasing to 169 wild adults at the end of the 2023–2024 breeding season. Here we use mitogenomes to enable comparisons of diversity between contemporary and historical (pre-1960s) stilts, and to understand the impacts of past interspecific hybridisation. We assemble a mitogenome for kakī and use this as a reference to facilitate downstream comparisons of mitochondrial diversity among kakī and poaka across a period of population decline and subsequent conservation management for kakī. Mitogenome haplotype data provides no evidence of introgression from poaka into kakī despite past hybridisation. This contributes to the behavioural, ecological, morphological and genetic evidence that conservation action has maintained the species integrity of this Critically Endangered bird. Furthermore, these results indicate that mitochondrial diversity has been maintained in kakī across a period of species decline and subsequent conservation management.

The Southern Ocean is warming more rapidly than other parts of our planet. How this region’s endemic biodiversity will respond to such changes can be illuminated by studying past events, through genetic analyses of time-series data sets including historic and fossil remains. Archaeological and subfossil remains show that the southern elephant seal ( Mirounga leonina ) was common along the coasts of Australia and New Zealand in the recent past. This species is now mostly confined to sub-Antarctic islands and the southern tip of South America. We analysed ancient seal samples from Australia (Tasmania), New Zealand, and the Antarctic mainland to examine how southern elephant seals have responded to a changing climate and anthropogenic pressures during the Holocene. Our analyses show that these seals formed part of a broader Australasian lineage, comprising seals from all sampled locations from the south Pacific sector of the Southern Ocean. Our study demonstrates that southern elephant seal populations have dynamically altered both range and population sizes under climatic and human pressures, over surprisingly short evolutionary timeframes for such a large, long-lived mammal. Significance Statement Genetic data, alongside historic, archaeological, and subfossil remains show that Australasian populations of the southern elephant seal have been shaped by range expansions and contractions following the Last Glacial Maximum, with subsequent contractions during the late Holocene. These expansion and contraction events are likely to have been a direct result of climate change-induced habitat expansion and contraction, along with Indigenous and European sealing. Prehistoric climate change and more recent human pressures have substantially altered the geographic distribution and population size of southern elephant seals over short evolutionary timescales.

Population genetic data is often essential to inform conservation management. Understanding the distribution of genetic variants within and between populations can reveal novel insights into genetic connectivity and evolutionary processes. However, obtaining such data using invasive approaches such as tissue sampling may negatively affect the very species we are seeking to protect. Thus, interest in using non-invasive environmental DNA (eDNA) techniques for identifying genetic variation within target species populations has grown. Along with this interest comes the desire to expand the amount of population genetic information that can be obtained from eDNA to increasingly large fragments of the genome, such as entire mitogenomes. Here, we introduce an eDNA hybridisation capture approach to sequencing complete mitochondrial genomes of New Zealand fur seals (Arctocephalus forsteri) (Māori: kekeno) from marine water samples. We show that our approach can recover up to 99% of the fur seal mitogenome. Furthermore, we present a pipeline to extract haplotype diversity from such eDNA population genetic data. Haplotypic variation identified using this approach matches previously identified patterns of intraspecific genetic variation from fur seal tissue samples, suggesting that eDNA methods can accurately identify mitochondrial variation. Our study demonstrates that whole mitogenomes can be recovered using hybridisation capture enrichment of eDNA and indicates that eDNA may be a promising tool for population genetics. Within this context, we discuss some of the key challenges that must be overcome before the promise of eDNA can be fully realized.

The origin and evolution in the Southern Hemisphere of the Austral teals, consisting of the grey-teal and brown-teal species complexes, remains poorly understood owing to limited molecular data. With the group containing multiple independent examples of flight loss, understanding the evolutionary history of the group is of significant interest for functional genomic studies into the evolution of flightlessness. Here, we present the first whole-mitogenome-based phylogeny of the Austral teals. We show that the group diverged from a common ancestor with mallards in the late Miocene and soon after radiated into the brown-teal and grey-teal lineages, in addition to the widely distributed pintails and green-winged teals. The brown-teal species complex, which includes the volant brown teal, the flight-impaired, sub-Antarctic Auckland Island teal, and the flightless, Chatham Island and sub-Antarctic Campbell Island teals, radiated within the past 0.9–1.8 Myr. The divergence of the extinct Chatham Island teal and the colonization of the Auckland and Campbell Islands occurred from mainland New Zealand. Morphological changes towards flightlessness are also present in the volant brown teal on mainland New Zealand, suggesting that this group was on the pathway to flightlessness, a trend that accelerated in some insular island lineages.

Marine sponges have recently emerged as efficient natural environmental DNA (eDNA) samplers. The ability of sponges to accumulate eDNA provides an exciting opportunity to reconstruct contemporary communities and ecosystems with high temporal and spatial precision. However, the use of historical eDNA, trapped within the vast number of specimens stored in scientific collections, opens up the opportunity to begin to reconstruct the communities and ecosystems of the past. Here, we define the term ‘heDNA’ to denote the historical environmental DNA that can be obtained from the recent past with high spatial and temporal accuracy. Using a variety of Antarctic sponge specimens stored in an extensive marine invertebrate collection, we were able to recover information on Antarctic fish biodiversity from specimens up to 20 years old. We successfully recovered 64 fish heDNA signals from 27 sponge specimens. Alpha diversity measures did not differ among preservation methods, but sponges stored frozen had a significantly different fish community composition compared to those stored dry or in ethanol. Our results show that we were consistently and reliably able to extract the heDNA trapped within marine sponge specimens, thereby enabling the reconstruction and investigation of communities and ecosystems of the recent past with a spatial and temporal resolution previously unattainable. Future research into heDNA extraction from other preservation methods, as well as the impact of specimen age and collection method, will strengthen and expand the opportunities for this novel resource to access new knowledge on ecological change during the last century.

Mitochondrial genomes (mitogenomes) represent a relatively cost-effective tool for comparing diversity between contemporary and historical populations to assess impacts of past population processes, or the outcomes of conservation management. The Aotearoa New Zealand endemic kakī | black stilt ( Himantopus novaezelandiae ) is a critically endangered wading bird. Anthropogenic impacts contributed to kakī declining to ~ 23 individuals in 1981 and promoted interspecific hybridisation with their more common congener, the poaka | pied stilt ( H. himantopus leucocephalus ). Conservation management of kakī has resulted in the population increasing to 169 wild adults today. Here we use mitogenomes to enable comparisons of diversity between contemporary and historical (pre-1970s) stilts, and to understand the impacts of past interspecific hybridisation. We assemble a mitogenome for kakī and use this as a reference to facilitate downstream comparisons of mitochondrial diversity among kakī and poaka through time. Mitogenome haplotypes clearly differentiate kakī from poaka, and thus contribute to the behavioural, ecological, morphological and genetic evidence that conservation action has maintained the species integrity of this critically endangered bird. Furthermore, these results indicate conservation management aiming to maintain genetic diversity has been successful.

Marine sponges have recently emerged as efficient natural environmental DNA (eDNA) samplers. The ability of sponges to accumulate eDNA provides an exciting opportunity to reconstruct contemporary communities and ecosystems with high temporal and spatial precision. However, the use of historical eDNA (heDNA), trapped within the vast number of specimens stored in scientific collections, opens up the opportunity to begin to reconstruct the communities and ecosystems of the past. Here, using a variety of Antarctic sponge specimens stored in an extensive marine invertebrate collection, we were able to recover information on Antarctic fish biodiversity from specimens up to 20 years old. We successfully recovered 64 fish heDNA signals from 27 sponge specimens. Alpha diversity measures did not differ among preservation methods, but sponges stored frozen had a significantly different fish community composition compared to those stored dry or in ethanol. Our results show that we were consistently and reliably able to extract the heDNA trapped within marine sponge specimens, thereby enabling the reconstruction and investigation of communities and ecosystems of the recent past with a spatial and temporal resolution previously unattainable. Future research into heDNA extraction from other preservation methods, as well as the impact of specimen age and collection method will strengthen and expand the opportunities for this novel resource to access new knowledge on ecological change during the last century.

Effective management of biodiversity requires regular surveillance of multiple species. Analysis of environmental DNA (eDNA) by metabarcoding holds promise to achieve this relatively easily. However, taxonomy‐focused eDNA surveys need suitable molecular reference data, which are often lacking, particularly at the species level and for remote locations. To evaluate the comparability of environmental DNA surveys and traditional surveys in a real‐life case study in a marine area of high conservation value, we conducted a biodiversity survey of the fish in remote and pristine Te Wāhipounamu/Fiordland (Aotearoa/New Zealand), incorporating multiple data sources. We compared eDNA‐derived species identifications against Baited Remote Underwater Video (BRUV) data collected at the same time and locations as eDNA. We also cross‐referenced both eDNA and BRUV data against literature and the Ocean Biodiversity Information System (OBIS), with literature and OBIS data representing a summary of multiple traditional surveying approaches. In total, we found 116 fish species in our study area. Environmental DNA detected 43 species; however, only three of those species overlap with species known from the literature, OBIS, or our BRUV analyses. A total of 61 fish species were known from the region from the literature, while OBIS listed 28 species, and our BRUV analyses picked up 26 species. BRUV data coincided more strongly than eDNA data with literature and OBIS data. Twenty of the 26 species detected by BRUV were known from literature and OBIS. We argue that limitated DNA reference databases are the main cause of this discrepancy, and our results indicate that eDNA of rare and endangered species can be detected if matching reference data were available. Environmental DNA analyses can only identify species present among reference data and with relaxed taxonomic assignment parameters may converge on relatives of detected species if the actually existing species themselves are missing among reference data. However, the high number of species detected by our eDNA analyses confirms that eDNA could be a powerful tool for biodiversity surveys if suitable investments in local reference databases were made.