Full Mitogenomes in the Critically Endangered Kākāpō Reveal Major Post-Glacial and Anthropogenic Effects on Neutral Genetic Diversity

Abstract

Understanding how species respond to population declines is a central question in conservation and evolutionary biology. Population declines are often associated with loss of genetic diversity, inbreeding and accumulation of deleterious mutations, which can lead to a reduction in fitness and subsequently contribute to extinction. Using temporal approaches can help us understand the effects of population declines on genetic diversity in real time. Sequencing pre-decline as well as post-decline mitogenomes representing all the remaining mitochondrial diversity, we estimated the loss of genetic diversity in the critically endangered kākāpō (Strigops habroptilus). We detected a signal of population expansion coinciding with the end of the Pleistocene last glacial maximum (LGM). Also, we found some evidence for northern and southern lineages, supporting the hypothesis that the species may have been restricted to isolated northern and southern refugia during the LGM. We observed an important loss of neutral genetic diversity associated with European settlement in New Zealand but we could not exclude a population decline associated with Polynesian settlement in New Zealand. However, we did not find evidence for fixation of deleterious mutations. We argue that despite high pre-decline genetic diversity, a rapid and range-wide decline combined with the lek mating system, and life-history traits of kākāpō contributed to a rapid loss of genetic diversity following severe population declines.

Keywords: bottleneck; endemic; expansion; genetic diversity; historical DNA; mitogenome.

Figure 1

Temporal haplotype network displaying the change in mitogenome (16,588 bp) diversity through time for historical (in blue, bottom part; n = 39) and modern (in grey, top part; n = 79) kākāpō samples. Circles represent haplotypes and numbers represent sample sizes. Empty circles represent absent haplotypes for a given time period. Haplotypes found in multiple time periods are connected by vertical lines. Within each time period, black dots represent one mutation.

Figure 2

Bayesian phylogeny in kākāpō for full mitogenomes (16,588 bp). Timing of events was estimated assuming a substitution rate of 1–3 × 10⁻⁸ site⁻¹ year⁻¹ [39]. The x-axis is in calendar years before present and nodes with posterior probability larger than 0.7 are depicted. Maps show the extent of ice during (white) and after the last glacial maximum (LGM) (after [49]).

Figure 3

(a) Sampling locations for 39 historical and 79 modern kākāpō. Full circles represent sampling locations for historical specimens only and split circles refer to sampling locations for both historical specimens and modern birds. Numbers represent sample sizes for each location and dataset. Stars represent geographic origin of the founders. (b) Median-joining haplotype network for 118 kākāpō mitogenomes (16,588 bp). Geographical locations in the legend are listed from north to south.

Figure 4

Bayesian Skyline plot (BSP) depicting population size change through time in kākāpō for full mitogenomes (16,588 bp). Timing of events was estimated assuming a substitution rate of 1–3 × 10⁻⁸ site⁻¹ year⁻¹ [39]. The x axis is in calendar years before present and y axis equals changes in effective population size (shown as the product of N_e and generation time T). The black line is the median estimate and the blue lines show the 95% highest posterior density intervals.