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

Wyatt KB, Campos PF, Gilbert MT, Kolokotronis SO, Hynes WH, DeSalle R, Ball SJ, Daszak P, MacPhee RD, Greenwood AD - PLoS ONE (2008)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Biological Sciences Department, Old Dominion University, Norfolk, VA, USA.

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.

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Related in: MedlinePlus

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.
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pone-0003602-g002: 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.

Mentions: Sequences were obtainable from all 18 rat samples (100% success rate) with the RAG1 A primers. On the basis of fixed differences in recovered cytochrome b and RAG1 sequences (Table 2), we determined that the samples could be exhaustively divided into two groups. More precisely, modern Rattus rattus and the alleged hybrids were found to differ in a distinct and consistent manner from specimens designated as R. macleari on museum labels, with little or no within-group variation (0-2 difference per fragment) (Table 2). Given the lack of within-group differences for RAG 1A, genes RAG 1 B, GHR A and B were sampled in a subset of specimens, with identical results, as determined by comparing recovered sequences to those for R. rattus in GenBank and by performing relevant phylogenetic analysis (Fig. 2). Results with the different genes gave a consistent result indicating R. macleari was indeed distinct from R. rattus. We conclude that the absence of consistent genetic differences between R. rattus and the putative hybrids indicates that the latter are simply morphological variants of the former, which is consistent with the observation that R. rattus is a notably polymorphic species [13]. If intensive hybridization had actually occurred, it would have had to happen within a very short period, as the endemic rats became extinct within a maximum of 9 years subsequent to black rat introduction. In any case, it would be expected that at least some individuals—and in particular the morphological hybrids—would harbor alleles from both species: no evidence of this can be seen in the genetic information available.


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

Wyatt KB, Campos PF, Gilbert MT, Kolokotronis SO, Hynes WH, DeSalle R, Ball SJ, Daszak P, MacPhee RD, Greenwood AD - PLoS ONE (2008)

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.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2572834&req=5

pone-0003602-g002: 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.
Mentions: Sequences were obtainable from all 18 rat samples (100% success rate) with the RAG1 A primers. On the basis of fixed differences in recovered cytochrome b and RAG1 sequences (Table 2), we determined that the samples could be exhaustively divided into two groups. More precisely, modern Rattus rattus and the alleged hybrids were found to differ in a distinct and consistent manner from specimens designated as R. macleari on museum labels, with little or no within-group variation (0-2 difference per fragment) (Table 2). Given the lack of within-group differences for RAG 1A, genes RAG 1 B, GHR A and B were sampled in a subset of specimens, with identical results, as determined by comparing recovered sequences to those for R. rattus in GenBank and by performing relevant phylogenetic analysis (Fig. 2). Results with the different genes gave a consistent result indicating R. macleari was indeed distinct from R. rattus. We conclude that the absence of consistent genetic differences between R. rattus and the putative hybrids indicates that the latter are simply morphological variants of the former, which is consistent with the observation that R. rattus is a notably polymorphic species [13]. If intensive hybridization had actually occurred, it would have had to happen within a very short period, as the endemic rats became extinct within a maximum of 9 years subsequent to black rat introduction. In any case, it would be expected that at least some individuals—and in particular the morphological hybrids—would harbor alleles from both species: no evidence of this can be seen in the genetic information available.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Biological Sciences Department, Old Dominion University, Norfolk, VA, USA.

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.

Show MeSH
Related in: MedlinePlus