Analysis of Genomic Sequence Data Reveals the Origin and Evolutionary Separation of Hawaiian Hoary Bat Populations

We examine the genetic history and population status of Hawaiian hoary bats (Lasiurus semotus), the most isolated bats on Earth, and their relationship to northern hoary bats (Lasiurus cinereus), through whole-genome analysis of single-nucleotide polymorphisms mapped to a de novo-assembled reference genome. Profiles of genomic diversity and divergence indicate that Hawaiian hoary bats are distinct from northern hoary bats, and form a monophyletic group, indicating a single ancestral colonization event 1.34 Ma, followed by substantial divergence between islands beginning 0.51 Ma. Phylogenetic analysis indicates Maui is central to the radiation across the archipelago, with the southward expansion to Hawai‘i and westward to O‘ahu and Kaua‘i. Because this endangered species is of conservation concern, a clearer understanding of the population genetic structure of this bat in the Hawaiian Islands is of timely importance

Genetic diversity, structure, and effective population size of an endangered, endemic hoary bat, ʻōpeʻapeʻa, across the Hawaiian Islands

Island bat species are disproportionately at risk of extinction, and Hawaiʻi’s only native terrestrial land mammal, the Hawaiian hoary bat (Lasiurus semotus) locally known as ʻōpeʻapeʻa, is no exception. To effectively manage this bat species with an archipelago-wide distribution, it is important to determine the population size on each island and connectivity between islands. We used 18 nuclear microsatellite loci and one mitochondrial gene from 339 individuals collected from 1988–2020 to evaluate genetic diversity, population structure and estimate effective population size on the Islands of Hawaiʻi, Maui, Oʻahu, and Kauaʻi. Genetic differentiation occurred between Hawaiʻi and Maui, both of which were differentiated from Oʻahu and Kauaʻi. The population on Maui presents the greatest per-island genetic diversity, consistent with their hypothesized status as the original founding population. A signature of isolation by distance was detected between islands, with contemporary migration analyses indicating limited gene flow in recent generations, and male-biased sex dispersal within Maui. Historical and long-term estimates of genetic effective population sizes were generally larger than contemporary estimates, although estimates of contemporary genetic effective population size lacked upper bounds in confidence intervals for Hawaiʻi and Kauaʻi. Contemporary genetic effective population sizes were smaller on Oʻahu and Maui. We also detected evidence of past bottlenecks on all islands with the exception of Hawaiʻi. Our study provides population-level estimates for the genetic diversity and geographic structure of ‘ōpeʻapeʻa, that could be used by agencies tasked with wildlife conservation in Hawaiʻi

Sampling locations.

<p>The locations for <i>L</i>. <i>cinereus</i> specimens used in <i>CO1</i> analysis.</p

Maximum parsimony network of <i>CO1</i> haplotypes.

<p>Each haplotype is represented by a circle, the relative size of which roughly corresponds to the haplotype frequency. The number of mutations between haplotypes is indicated only for those connections spanning more than one mutation. Hawaii1 haplotypes grey, Hawaii2/North America haplotypes white, South American haplotype black. Hawaiian islands haplotypes in bold.</p

Average pairwise genetic distances (<i>COI</i>) within and between <i>COI</i> clades.

<p>Average pairwise genetic distances (<i>COI</i>) within and between <i>COI</i> clades.</p

Extended Bayesian skyline plots for Hawaiian populations.

<p>Results of three runs are shown as gray lines, bounded by 95% confidence intervals in black. A. Skyline plot for the Hawaii1 population, showing a pattern of population growth starting at ca. 10 kya. B. Skyline plot for the Hawaii2 population, fitting a model of population stasis.</p