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

Abstract

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 kākāpō (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 Māori subsistence practices but also provides a more nuanced snapshot of anthropogenic impacts on native fauna after first human arrival.

Keywords: ancient DNA; bulk bone metabarcoding; human impacts; paleoecology; subsistence practices.

Fig. 1.

Overall biodiversity of excavated bulk bone. Species composition was analyzed using four metabarcoding assays targeting vertebrate taxa. (A) Dendrogram highlighting the diversity of orders identified in all samples, with examples of taxa identified in silhouettes. Bar sizes represent the number of taxa identified in each order. (B) Sample localities of archaeological midden sites (red triangles) and paleontological deposits (gray triangles). (C) Correspondence analysis based on presence/absence of all taxa identified from archaeological or paleontological sites. The distribution of herpetofauna (Class: Amphibia and Reptilia), fish species (Class: Actinopterygii and Chondrichthyes), and marine mammals (Family: Phocidae and Otariidae and Order: Cetacea) is highlighted by ellipses of incremental confidence intervals of 0.4, 0.6, and 0.8.

Fig. 2.

Localities of midden sites in which DNA from marine mammals was identified.

Fig. 3.

Geographic trends in archaeological fish assemblages. Coordination analysis of fish species composition from North Island and South Island assemblages based on presence/absence data, with the latitude of each site overlaid on the plot. The five most extreme taxa on the second axis (CA1) detected at more than one site are highlighted (black dots and gray silhouettes) for high and low latitudes, respectively. Similarly, the most commonly identified taxon on each island is highlighted (black dots and black silhouettes). The distribution of all other taxa detected at more than one site is illustrated by gray dots.

Fig. 4.

Decline in kākāpō genetic diversity. Haplotype network of a 214-bp mitochondrial control region sequence from modern, historical, and prehistorical kākāpō populations. Gray circles indicate haplotypes identified from single source material in Bergner et al. (41), whereas colored haplotypes were identified from bulk bone samples generated in this study. Hatch marks represents the number of control region mutations between haplotypes. For modern and historical haplotypes, numbers in each circle represent number of individuals in each haplotype, whereas for the prehistorical samples, numbers indicate number of DNA extracts in which each haplotype has been detected.