Evolutionary genomics of endangered Hawaiian tree snails (Achatinellidae: Achatinellinae) for conservation of adaptive capacity

Melissa R Price; Michael G Hadfield; Ingrid S S Knapp; Robert J Toonen; Zac H Forsman

doi:10.7717/peerj.10993

Evolutionary genomics of endangered Hawaiian tree snails (Achatinellidae: Achatinellinae) for conservation of adaptive capacity

PeerJ. 2021 Apr 22:9:e10993. doi: 10.7717/peerj.10993. eCollection 2021.

Authors

Melissa R Price¹, Michael G Hadfield², Ingrid S S Knapp³, Robert J Toonen³, Zac H Forsman³

Affiliations

¹ Department of Natural Resources and Environmental Management, University of Hawai'i at Mānoa, Honolulu, HI, USA.
² Kewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawai'i at Mānoa, Honolulu, HI, USA.
³ Hawai'i Institute of Marine Biology, University of Hawai'i at Mānoa, Kāne'ohe, HI, USA.

Abstract

Phylogenomic studies can provide insights into speciation, adaptation, and extinction, while providing a roadmap for conservation. Hawaiian tree snails are a model system for an adaptive radiation facing an extinction crisis. In the last 5 years, nearly all populations of Hawaiian tree snails across the 30 remaining species in the subfamily Achatinellinae (Achatinellidae) have declined from hundreds or thousands in the wild down to undetectable levels. Nearly 100 species historically occurred across dramatic environmental gradients on five of the Hawaiian Islands, but habitat loss, overcollection, and predation by invasive species have decimated populations. As such, this system offers the opportunity to integrate efforts to conserve evolutionary potential into conservation planning for a rapidly declining subfamily. Here, we used genome-wide, restriction-site associated DNA sequencing (RADseq), along with mitochondrial genome reconstruction, to resolve evolutionary relationships to inform conservation efforts. Phylogenetic analysis of nearly 400k genome-wide SNPs from 59 populations and 25 species across six genera in the family Achatinellidae, was generally concordant with taxonomy, geography, and mtDNA with several notable exceptions; mtDNA was unable to resolve some deeper nodes (e.g., the monophyly of Achatinella), while SNP data did not resolve as many shallow nodes. Both phylogenetic and coalescent analysis revealed deep divergences between populations within Achatinella mustelina that were consistent with species-level differences. Given cryptic species-level divergence within populations that are geographically proximate, they are at higher risk of extirpation from invasive predators and climate change than previously assumed. This study clarifies evolutionary relationships within this model system for adaptive radiation, forming the basis for conservation strategies such as translocation, captive rearing, and hybridization trials to prevent the loss of capacity to adapt to rapidly changing environmental conditions.

Keywords: Captive rearing; Colonization; Conservation genetics; Island species radiation; Mitochondrial genome; Phylogenomics; RADseq; Translocation.

Grants and funding

The project was funded by the Hawai‘i Division of Forestry and Wildlife, Department of Land and Natural Resources Grant Number C60886; and the Army Corps of Engineers with the Oahu Army Natural Resources Program under Cooperative Agreement Number W911KB-14-2-0001 TO 0004, under a subaward from the University of Alaska, Anchorage. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.