Historical mammal extinction on Christmas Island (Indian Ocean) correlates with introduced infectious disease

Abstract

It is now widely accepted that novel infectious disease can be a leading cause of serious population decline and even outright extinction in some invertebrate and vertebrate groups (e.g., amphibians). In the case of mammals, however, there are still no well-corroborated instances of such diseases having caused or significantly contributed to the complete collapse of species. A case in point is the extinction of the endemic Christmas Island rat (Rattus macleari): although it has been argued that its disappearance ca. AD 1900 may have been partly or wholly caused by a pathogenic trypanosome carried by fleas hosted on recently-introduced black rats (Rattus rattus), no decisive evidence for this scenario has ever been adduced. Using ancient DNA methods on samples from museum specimens of these rodents collected during the extinction window (AD 1888-1908), we were able to resolve unambiguously sequence evidence of murid trypanosomes in both endemic and invasive rats. Importantly, endemic rats collected prior to the introduction of black rats were devoid of trypanosome signal. Hybridization between endemic and black rats was also previously hypothesized, but we found no evidence of this in examined specimens, and conclude that hybridization cannot account for the disappearance of the endemic species. This is the first molecular evidence for a pathogen emerging in a naïve mammal species immediately prior to its final collapse.

Figure 1. Extinction time line for Christmas Island rats (background drawing of R. macleari by Patricia Wynne).

Figure 2. Phylogenetic relationships within tribe Rattini (Muridae: Murinae) based on cytochrome b (A), RAG1 (B), and GHR (C) coding sequences including the nucleotide sequences produced in this study.

All trees were estimated in a maximum likelihood framework. Scale bars denote substitutions per site along the branches. Shown in red and green are the rat sequences obtained in this study. The subtree corresponding to the Rattus species group sensu lato is colored in blue for clarity.

Figure 3. Phylogenetic relationships among trypanosome sequences bases on 18S rDNA sequences.

Scale bars denote substitutions per site along branches. Blue-colored sequences are the trypanosome sequences obtained in this study.