House mouse colonization patterns on the sub-Antarctic Kerguelen Archipelago suggest singular primary invasions and resilience against re-invasion

Abstract

BackgroundStarting from Western Europe, the house mouse (Mus musculus domesticus) has spread across the globe in historic times. However, most oceanic islands were colonized by mice only within the past 300 years. This makes them an excellent model for studying the evolutionary processes during early stages of new colonization. We have focused here on the Kerguelen Archipelago, located within the sub-Antarctic area and compare the patterns with samples from other Southern Ocean islands.ResultsWe have typed 18 autosomal and six Y-chromosomal microsatellite loci and obtained mitochondrial D-loop sequences for a total of 534 samples, mainly from the Kerguelen Archipelago, but also from the Falkland Islands, Marion Island, Amsterdam Island, Antipodes Island, Macquarie Island, Auckland Islands and one sample from South Georgia. We find that most of the mice on the Kerguelen Archipelago have the same mitochondrial haplotype and all share the same major Y-chromosomal haplotype. Two small islands (Cochons Island and Cimetière Island) within the archipelago show a different mitochondrial haplotype, are genetically distinct for autosomal loci, but share the major Y-chromosomal haplotype. In the mitochondrial D-loop sequences, we find several single step mutational derivatives of one of the major mitochondrial haplotypes, suggesting an unusually high mutation rate, or the occurrence of selective sweeps in mitochondria.ConclusionsAlthough there was heavy ship traffic for over a hundred years to the Kerguelen Archipelago, it appears that the mice that have arrived first have colonized the main island (Grande Terre) and most of the associated small islands. The second invasion that we see in our data has occurred on islands that are detached from Grande Terre and were likely to have had no resident mice prior to their arrival. The genetic data suggest that the mice of both primary invasions originated from related source populations. Our data suggest that an area colonized by mice is refractory to further introgression, possibly due to fast adaptations of the resident mice to local conditions.

Increased mitochondrial mutation frequency after an island colonization: positive selection or accumulation of slightly deleterious mutations?

“…Mutations in the full mitochondrial genome sequences occurred at the same frequency as in our previous survey of D-loop sequences [7]. In that survey, we found eight point mutations in 258 540 nt sequenced (310 animals  834 nt).…”

“…Positive selection has indeed been observed in very recently differentiated populations, in particular for ND2 and ND6 in the context of high-altitude adaptations [4 -6]. In a previous study, we found that mouse (Mus musculus domesticus) populations that had colonized sub-Antarctic islands less than 200 years ago showed a high number of substitutions in mitochondrial D-loop sequences [7]. This raised the question of whether positive selection could explain this pattern, because the mice on subAntarctic islands may have had to adapt to a feral lifestyle in a colder climate with new food resources.…”

Phylogeny and adaptation shape the teeth of insular mice

“…(i) Orkney nested into a mostly Scandinavian and British haplogroup [16], which has been interpreted as the signature of a Norwegian Viking colonization. (ii) Guillou shared its only haplotype with other mice from Kerguelen Archipelago and Western European specimens from England, Germany and France, and from harbours on the way to the Southern Ocean as in Cameroon [25]. [14].…”

“…DNA was extracted from ethanol-preserved tissue of Orkney mice, using the DNeasy Blood and Tissue kit (Qiagen, France). The D-loop was amplified using previously described primers and protocol [25]. The sequences generated were visualized using MEGA6 [26].…”

Cryptic diversity in Black rats Rattus rattus of the Galápagos Islands, Ecuador

“…The resilience of island populations of invasive rodents to re‐invasion has also been observed in M. musculus on the sub‐Antarctic Kerguelen archipelago (Hardouin et al. 2010). The authors of this study suggest that populations on small islands can become more quickly ecologically and genetically isolated than mice on the mainland.…”