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

BMC Evolutionary Biology House mouse colonization patterns on the sub-Antarctic Kerguelen Archipelago suggest singular primary invasions and resilience against re-invasion Emilie A Hardouin 0 Jean-Louis Chapuis Mark I Stevens Jansen Bettine van Vuuren Petra Quillfeldt Rick J Scavetta 0 Meike Teschke 0 Diethard Tautz 0 0 Max Planck Institute of Evolutionary Biology , August-Thienemann-Str. 2, 24306 Plon , Germany Background: Starting 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. Results: We 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 Cimetire 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. Conclusions: Although 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. - Background Island colonization dynamics are of general interest in evolutionary biology, both with respect to understanding adaptive radiations, as well as for tracing migration patterns. In this context it is of particular interest to ask whether a single colonization can already result in a new established population that is refractory to further invasions, or whether multiple independent invaders are required before a new stable population can be established. This question can be particularly well studied in cases of recent island colonization, since this provides insights into the early phases of establishment and adaptation in a population context. The spread of the house mouse (Mus musculus L.) across many oceanic islands in contemporary times constitutes an excellent model system in this respect [1,2]. Mus musculus originated on the Indian subcontinent within the past million years and there are currently at least three recognized subspecies: M. m. domesticus, M. m. musculus, M. m. castaneus [3]. M. m. domesticus invaded Western Europe about 3,000 years ago [4] and then colonized the rest of the world (i.e. Africa, America and Australia/New Zealand) mostly in the wake of increased human travel across the globe that started in the 16th century [1,3,4]. They were also very successful in colonizing isolated islands, such as those of the Southern Ocean [5-9], where they were brought by whaling ships making stops during their journeys or went for seal hunting. The Kerguelen archipelago was discovered on the 12th of February 1772 by Yves-Joseph de KerguelenTrmarec. It is situated about 4,000 km away from the African and the Australia coast (Figure 1a), has a large main island of 6,500 km2 called Grande Terre, and approximately 60 small islands (1-200 km2) surrounding it (Figure 1b). The climate is Oceanic cold, characterized by cold summers (8C on average), no rigorous winters (2C on average), by strong wind and mean annual rainfall of 747 mm (350-1479 mm during 1951-2009, Mto-France, Port-aux-Franais). There was never an extended human settlement on the archipelago, but since 1951, there is a research and weather station with a continuous turnover of about 60 to 120 people per year. The house mouse was most likely introduced to the Kerguelen at the beginning of the 19th century [10-12], but certainly not before 1772, since it is too far away from the continents to have been a destination for ship traffic in previous times. During the high times of whale and seal hunting, there was heavy boat traffic in this area, with a large potential to bring additional mice. Today, the mice have colonized all of Grande Terre as well as many of the small islands of the Morbihan Gulf [13,14]. With this defined history, as well as extensive data on the genetic diversity of the relevant source populations (Western Europe), we have an excellent test case to study population genetic consequences of island invasion, the subsequent spread to further islands and patterns of re-invasion. Results Mitochondrial Data We sequenced 834 bp of the mitochondrial control region (D-loop) from all samples and found that all haplotypes grouped within the known M. m. domesticus haplotypes (Figure 2a), i.e. belong to this subspecies. This was already known for some of the islands [8,9] and we show here that it is also the case for the Kerguelen Archipelago, Amsterdam Island, Falkland Islands and South Georgia. Hence, the source populations of the mice colonizing the small Southern Ocean islands came most likely from Western Europe, or via Atlantic Figure 1 Locations of the Southern Ocean islands assessed in this study (left) and map of the Kerguelen Archipelago (right). The sampling sites in the Kerguelen Archipelago are all around the Morbihan Gulf and the research station at Port-aux-Franais except PortCouvreux, Pointe du Morne and the Cap Ratmanoff (see further details in Figure 5). Figure 2 D-loop haplotype networks calculated using Median Joining for M. m. domesticus samples with M. m. musculus as outgroup. The size of the circles represents the frequency of the respective haplotype in our sample. Each node is one mutational step away from the next node, numbers indicate the cases where more than one step is required to join the nodes. Small red circles indicate branch splits. (A) General network including all published sequences that are related to the Kerguelen haplotypes. (B) Same network as (...truncated)