Demographic decline and lineage-specific adaptations characterize New Zealand kiwi

Abstract

Small and fragmented populations may become rapidly differentiated due to genetic drift, making it difficult to distinguish whether neutral genetic structure is a signature of recent demographic events, or of long-term evolutionary processes that could have allowed populations to adaptively diverge. We sequenced 52 whole genomes to examine Holocene demographic history and patterns of adaptation in kiwi ( Apteryx ), and recovered 11 strongly differentiated genetic clusters corresponding to previously recognized lineages. Demographic models suggest that all 11 lineages experienced dramatic population crashes relative to early- or mid-Holocene levels. Small population size is associated with low genetic diversity and elevated genetic differentiation ( F ST ), suggesting that population declines have strengthened genetic structure and led to the loss of genetic diversity. However, population size is not correlated with inbreeding rates. Eight lineages show signatures of lineage-specific selective sweeps (284 sweeps total) that are unlikely to have been caused by demographic stochasticity. Overall, these results suggest that despite strong genetic drift associated with recent bottlenecks, most kiwi lineages possess unique adaptations and should be recognized as separate adaptive units in conservation contexts. Our work highlights how whole-genome datasets can address longstanding uncertainty about the evolutionary and conservation significance of small and fragmented populations of threatened species.

Genomic insights into the evolutionary relationships and demographic history of kiwi

“…Such a low number of founders would undoubtedly lead to high levels of inbreeding. However, this is in contrast to a lack of signs of inbreeding suggested by a recent population genomic study [15]; we suggest this may be a byproduct of the computational approach employed in the study, rather than a biological signal. Mapping to a phylogenetically distant reference has been shown to essentially remove signs of inbreeding [34].…”

“…Our finding of very low diversity in little spotted kiwi is congruent with previous studies based on microsatellite data [40] and population-level nuclear genomes [15]. Our finding of low diversity in this species -at least as represented by our sampled individualmay reflect the high levels of inbreeding we uncovered, putatively due to the recent history of this species.…”

“…We recovered phylogenetic relationships among the five kiwi species consistent with previous research using mtDNA sequences and nuclear data [3,7,15,35](Fig. 1).…”

“…Mapping to a phylogenetically distant reference has been shown to essentially remove signs of inbreeding [34]. Bemmels et al (2021) did not map the little spotted kiwi to a conspecific reference genome, and therefore the lack of inbreeding may be the result of mapping biases.…”

“…The use of genome-wide data can greatly enhance our existing understanding of kiwi relationships, as they allow analyses of species deep-time evolutionary histories. De novo nuclear genome assemblies are available from four of the five kiwi species (great spotted kiwi, little spotted kiwi, Okarito brown kiwi, North Island brown kiwi) [2,14], and resequencing data are available from the southern brown kiwi [15]. Here, we utilise single genome representatives of each species to better understand the interspecific evolutionary relationships among kiwi species, and to elucidate how past environmental changes (up to 1 Ma) may have impacted their demographic histories.…”