Apodemus sylvaticus, (Linnaeus, 1758)

A. sylvaticus (Linnaeus, 1758) View in CoL in northern Africa

( Libois et al., 2001) and A. agrarius (Pallas, 1771)

on the Danish islands Lolland and Faster ( Andersen et al., 2017), which is not typical for mice of the genus Apodemus . More than 100 species or subspecies of this genus have been established in the historical literature ( Thomas, 1922; Allen, 1938; Ellerman & Morrison-Scott, 1951; Xia, 1984; Musser et al., 1996; Musser & Carleton, 2005). Species of Apodemus are most abundant in the broadleaf forests of Palaearctic and Oriental areas. Several of these species host multiple human pathogens ( Klein et al., 2015; Ma et al., 2015), notably hantavirus ( Guzzetta et al., 2017; Tian et al., 2017) and Ljungan virus ( Hauffe et al., 2010). A study on the evolutionary history and dispersal of this genus is, therefore, important for public health and biodiversity conservation in Eurasia and North Africa.

Rapid radiation of Apodemus during the Late Miocene is thought to have been associated with global forest changes, when the flora changed from tropical to temperate during the Late Miocene ( Serizawa et al., 2000). The earliest fossil records of this genus and its sister genera were dated to the early Late Miocene, approximately 11 Mya ( Freudenthal, 1976; Martin Suarez & Mein, 1998; Kimura et al., 2017), but based on molecular data, the earliest divergence time of this genus was estimated to be approximately 6–8 Mya ( Michaux et al., 2002; Liu et al., 2004; Suzuki et al., 2008; Darvish et al., 2015). Three crucial evolutionary events of this genus were recognized in previous studies: (1) initial broad dispersal and radiation approximately 6 Mya, (2) regional radiation in Europe and China approximately 2 Mya and (3) westward dispersal of A. agrarius to Europe in the Quaternary ( Suzuki et al., 2008). These conclusions were proposed without evidence from fossil information or robust statistical analyses. A comprehensive study including extant and fossil species is important for understanding the evolutionary history of this genus.

According to the most comprehensive mammalian checklists, the composition of Apodemus is still disputable. Mammal species of the world and the Handbook of the mammals of the world listed 20 species of Apodemus ( Musser & Carleton, 2005; Wilson et al., 2016). Traditional taxonomy divided Apodemus into three groups: the Apodemus group, the Sylvaemus group and the Alsomys group ( Zimmermann, 1962) or the Argenteus group ( Musser et al., 1996). Studies based on complete mitochondrial cytochrome b (Cytb) sorted Apodemus species into four groups or subgenera: the Sylvaemus group [ A. uralensis (Pallas, 1811) , A. flavicolllis (Melchior, 1834) , A. alpicola Heinrich, 1952 , A. sylvaticus , A. mystacinus (Danford & Alston, 1877) , A. hermonensis (Filippucci et al., 1989) ], the Apodemus group [( A. agrarius , A. chevrieri (Milne-Edwards, 1868) , A. speciosus (Temminck, 1844) , A. draco (Barrett-Hamilton, 1900) , A. ilex Thomas, 1922 , A. semotus Thomas, 1908 , A. latronum Thomas, 1911 and A. peninsulae (Thomas, 1907) ] and A. argenteus (Temminck, 1844) and A. gurkha Thomas, 1924 , constitute two other distinct groups ( Serizawa et al., 2000; Liu et al., 2004; Suzuki et al., 2008). Generally, different aspects of species in Europe and eastern Asia have been well studied. For example, genetic variation among species using protein electrophoresis suggested a recent separation of members of the subgenus Sylvaemus from a common ancestor, followed by rapid radiation ( Filippucci et al., 2002), and higher genetic variability of field mice was found in the Mediterranean peninsulas than in northern Europe ( Michaux et al., 2003). Moreover, a large number of fossil species from Europe were described that were absent from glacial assemblages, but are always present in interglacial assemblages ( Martin Suarez & Mein, 1998; Knitlova & Horacek, 2017a, b). However, it is unclear how the evolutionary history of Apodemus formed its current distributional pattern.

Faunas in many regions of China remain relatively poorly explored, impeding a comprehensive understanding of interspecific differentiation. Allen (1938) recognized five species of Apodemus in China and Xia (1984) listed six: A. sylvaticus , A. draco , A. peninsulae , A. latronum , A. chevrieri and A. agrarius . Zheng (1993) reported fossil occurrences of A. chevrieri , A. agrarius , A. sylvaticus and A. cf. peninsulae that were dated to the Late Pleistocene in Chongqing and Guizhou Provinces. Based on a large number of Apodemus specimens from China, Musser et al. (1996) recognized seven species, A. agrarius , A. chevrieri , A. peninsulae , A. latronum , A. draco , A. semotus and A. uralensis , but excluded A. sylvaticus . Smith & Xie (2008) included one more species, A. pallipes (Barrett-Hamilton, 1900) , than the study of Musser et al. (1996), but this number was not followed by Wilson et al. (2016), detailed information are given in Table 1. In recent studies, A. ilex is also considered a distinct species ( Liu et al., 2004, 2012, 2017). A previous study based on a wider range of sampling, and using cytochrome oxidase subunit I ( Cox 1) recognized A. agrarius , A. chevrieri , A. peninsulae , A. latronum , A. ilex , A. draco and A. uralensis , and identified a distinct genetic lineage from Guizhou Province ( Liu et al., 2017). However, it is unclear how to identify these species based on morphology and a detailed description of the distinct genetic lineage is lacking. An integrative study on the phylogeny of Apodemus and taxonomy of species in this genus in China is, therefore, warranted.

In recent years, we collected a large number of samples of the genus Apodemus in China and examined collections in several museums that preserve Chinese specimens. Here, our aim is to (1) investigate the evolutionary history of this taxon by integrating fossil occurrences and extant species, (2) use the broadest geographic coverage of Apodemus to date, to assess the phylogenetic relationships and morphological variation of all species of this genus recorded in China and (3) test whether the newly discovered genetic lineage in our previous study represents a distinct species. By integrating molecular and morphological data, we established a new species of the genus Apodemus from high mountains in south-eastern China (27.83ºN, 108.76ºE).