Of mice and the ‘Age of Discovery’: the complex history of colonization of theAzorean archipelago by the house mouse (Mus musculus) as revealed by mitochondrialDNAvariation

Abstract

Humans have introduced many species onto remote oceanic islands. The house mouse (Mus musculus) is a human commensal and has consequently been transported to oceanic islands around the globe as an accidental stowaway. The history of these introductions can tell us not only about the mice themselves but also about the people that transported them. Following a phylogeographic approach, we used mitochondrial D-loop sequence variation (within an 849-to 864-bp fragment) to study house mouse colonization of the Azores. A total of 239 sequences were obtained from all nine islands, and interpretation was helped by previously published Iberian sequences and 66 newly generated Spanish sequences. A Bayesian analysis revealed presence in the Azores of most of the D-loop clades previously described in the domesticus subspecies of the house mouse, suggesting a complex colonization history of the archipelago as a whole from multiple geographical origins, but much less heterogeneity (often single colonization?) within islands. The expected historical link with mainland Portugal was reflected in the pattern of D-loop variation of some of the islands but not all. A more unexpected association with a distant North European source area was also detected in three islands, possibly reflecting human contact with the Azores prior to the 15th century discovery by Portuguese mariners. Widening the scope to colonization of the Macaronesian islands as a whole, human linkages between the Azores, Madeira, the Canaries, Portugal and Spain were revealed through the sharing of mouse sequences between these areas. From these and other data, we suggest mouse studies may help resolve historical uncertainties relating to the 'Age of Discovery'.

Genetic characterization of invasive house mouse populations on small islands

“…Individual-level ancestry profiles are consistent within geographically-defined populations on both the autosomes and X chromosome ( Figure S3 ), supporting the notion that islands are resistant to repeated invasions after the initial colonization event (Hardouin et al 2010; Jones et al 2011; Gabriel et al 2015). In a limited number of cases we can make a strong statement about the likely source population: Ruapuke appears to have been colonized from the eastern coast of Australia; Porto Santo from Portugal and Spain; and Heligoland from northern Germany ( Figure 3 ).…”

“…Individual-level ancestry profiles are consistent within geographically-defined populations on both the autosomes and X chromosome ( Figure S3 ), supporting the notion that islands are resistant to repeated invasions after the initial colonization event (Hardouin et al 2010;Jones et al 2011; Gabriel et al 2015). We find that mice from islands with historical connections to the British Isles, such as Antipodes, Auckland, Chatham and Pitt in the Southern Ocean, have greatest affinity to present-day populations from northern Europe (Scotland, Belgium, Germany) and to larger landmasses colonized by the British (Maryland, New Zealand) ( Figure 3 ; see also Veale et al (2018)).…”

“…Little is known about the origins, ancestry, or population structure of mice on either the Farallones or Floreana. Studies of several other offshore islands - Gough Island (Gray et al 2014), the Faroe Islands (Jones et al 2011), the Azores (Gabriel et al 2015), the Kerguelen Archipelago (Hardouin et al 2010), Antipodes (Searle et al 2009; Veale et al 2018), and Madeira (Gündüz et al 2001) - have revealed predominantly western European ancestry consistent with human-mediated dispersal by mariners within the past several centuries. Those studies relied heavily on mitochondrial sequences with or without a small number of nuclear microsatellite markers, and thus had limited resolution for population structure and inbreeding.…”

The genomic ancestry, landscape genetics, and invasion history of introduced mice in New Zealand

“…House mice have accompanied humans around the world for thousands of years [48]. Because of their highstanding genetic diversity, it has been possible to track the origins of introduced mouse populations [2], revealing activities and movements of people invisible to traditional historical methods [49][50][51][52][53]. New Zealand was entirely free of all terrestrial mammals until the introduction of the Pacific rat (Rattus exulans), which arrived with Polynesian settlement around 1280 AD [54].…”

Global population divergence and admixture of the brown rat (Rattus norvegicus)

“…The development of agriculture and resultant transition from nomadic to sedentary human societies created new ecological niches for species to evolve commensal or parasitic relationships with humans (Jones, et al 2013). The phylogeographic history of species living in close association with people often mirrors global patterns of human exploration (Searle, et al 2009; Gabriel, et al 2015) and colonization (Matisoo-Smith and Robins 2004; Cucchi, et al 2005; Suzuki, et al 2013; Hulme-Beaman, et al In Press). In particular, commensal rodent distributions have been strongly influenced by the movement of humans around the world.…”