Genetic Insights Into the Introduction History of Black Rats Into the Eastern Indian Ocean

Steve Donnellan,Philip J. Piper,Russell Palmer,Geoffrey Clark,Harriet Mills,Dave Algar,Atholl Anderson,Vicki A. Thomson,Steven Myers,Hitoshi Suzuki,Terry Bertozzi,Michael B. Herrera,Caitlyn Pink,Andrew S. Wiewel,Ken P. Aplin,Neil Hamilton

doi:10.3389/fevo.2021.786510

Abstract

Islands can be powerful demonstrations of how destructive invasive species can be on endemic faunas and insular ecologies. Oceanic islands in the eastern Indian Ocean have suffered dramatically from the impact of one of the world’s most destructive invasive species, the black rat, causing the loss of endemic terrestrial mammals and ongoing threats to ground-nesting birds. We use molecular genetic methods on both ancient and modern samples to establish the origins and minimum invasion frequencies of black rats on Christmas Island and the Cocos-Keeling Islands. We find that each island group had multiple incursions of black rats from diverse geographic and phylogenetic sources. Furthermore, contemporary black rat populations on these islands are highly admixed to the point of potentially obscuring their geographic sources. These hybridisation events between black rat taxa also pose potential dangers to human populations on the islands from novel disease risks. Threats of ongoing introductions from yet additional geographic sources is highlighted by genetic identifications of black rats found on ships, which provides insight into how recent ship-borne human smuggling activity to Christmas Island can negatively impact its endemic species.

Highlights

The invasive black rat (Rattus rattus) has a well-documented history of negative impacts on indigenous island fauna at a global scale (Towns et al, 2006), e.g., Indian Ocean – (Cheke and Jones, 1987), Mediterranean – (Martin et al, 2000; Ruffino et al, 2009), Atlantic – (Angel and Cooper, 2006), Pacific – (Atkinson, 1977; Spennemann, 1997)
MtClade I (n = 2, haplotypes = 1; H41-I) was found in both a forest location and a building on CXR, while mtClade II (n = 2, haplotypes = 2; H48-II and H77-II; Supplementary Figure 4 and Table 1) was found in built up areas and on an asylum-seeker vessel on CXR, and in Australia (H48-II) and Indonesia (H77-II)
When we examine the discordant mtClade I/Lineage IV CXR sample (ABTC136477 from Pink House that falls with the concordant mtClade IV/Lineage IV samples from CXR in the principal component analysis (PCA) in Figure 2), we note that it shares a rare mtClade haplotype (HAP 41-I) with the concordant mtClade I/Lineage I CXR sample, suggesting Mitochondrial DNA (mtDNA) capture of this rare mtClade I haplotype likely occurred on CXR

Summary

Introduction

The invasive black rat (Rattus rattus) has a well-documented history of negative impacts on indigenous island fauna at a global scale (Towns et al, 2006), e.g., Indian Ocean – (Cheke and Jones, 1987), Mediterranean – (Martin et al, 2000; Ruffino et al, 2009), Atlantic – (Angel and Cooper, 2006), Pacific – (Atkinson, 1977; Spennemann, 1997). Black Rats on Indian Islands in extinction events in this region e.g., the Mascarene and Seychelles groups (Towns et al, 2006), as well as major impacts on human health through disease transmission, e.g., plague on Madagascar (Rahelinirina et al, 2018). Common diseases known to infect black rats include Yersinia pestis (plague), Bartonella, Leptospirosis, Orientia tsutsugamushi (scrub typhus), Salmonella, and Hepatitis E (Kosoy et al, 2014). Novel recombinants of these or other diseases may pose risks to human populations if multiple black rat taxa come into contact outside of their native ranges (i.e., both on islands in the Indian Ocean as well as around the world)

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Discussion

Conclusion