Updated phylogeographic affinities within Dromiciops
Dromiciops distribution extends from the Chilean Pacific Coast in the west to the slopes of the Chilean Andes in the east and from the Maule Province at the north (35ºS) to the Palena Province at the South (44ºS) (Mejías et al., 2021; Oda, Rodríguez-Gómez, Fontúrbel, Soto-Gamboa, & Nespolo, 2019). In Argentina, Dromiciops is distributed along the Andes, from Neuquén to Chubut provinces (Figure 1). A small fraction of these habitats (7%, according to Martin, 2010) corresponds to the central valley of Chile (shrubland-type or Maulino forest habitats); while the temperate rainforest represents the remaining 93% of its distribution (Lobos, Charrier, Carrasco, & Palma, 2005; Martin, 2010; Saavedra & Simonetti, 2001; Uribe, Chiappe, & Estades, 2017). In addition to being drier than the typical wet rainforest, the habitats occupied in the Chilean central valley receive more sunlight and have more fruits available during the summer (Fontúrbel, Salazar, & Medel, 2017a). This distribution is much smaller than the past distribution of Microbiotheria, which encompassed Bolivia, Rio de Janeiro (Middle Palaeocene), Argentinian Patagonia, and the Seymour Island in Antarctica (Hershkovitz, 1999). Such distributional shrinking likely reflects major climatic changes, as the original Microbiotheria distribution (during the Miocene) was dominated by a subtropical-humid climate, similar to the present-day Dromiciopshabitat.
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The first phylogeographic analysis of Dromiciops populations was performed using two mitochondrial genes (Himes, Gallardo, & Kenagy, 2008), identifying three main clades that displayed geographic structure (northern: clade “A”, central: clade “B”, and southern: clade “C” clades). Most interestingly, this study reported sequence divergence between clades A and C of 11.3%, 15.1% between A and B, and 8.2% between B and C, markedly differentiated northern and southern clades later confirmed by Valladares-Gómez et al. (2019) using microsatellite markers. According to Himes et al. (2008), Dromiciops populations could have diverged in the Quaternary (1–1.8 Myr) before the last glacial maximum (~20,000 yr ago), but the deep divergence based on mitochondrial DNA suggests that these could be even older and paleontological evidence appears to agree with older divergences. Fossil evidence indicates that Dromiciops may be morphologically indistinguishable with Microbiotherium , a genus that lived between the late Oligocene and early Miocene (~29-16 Myr; Goin & Abello, 2013), which includes at least four extinct species and is considered the sister group ofDromiciops (Figure 2). Therefore, if Dromiciops is as old as these extinct lineages, this would suggest that the whole clade is as old as the Andes mountain range (Charrier, Pinto, & Rodríguez, 2006), and older than the scission of the Chiloé island (ca. 10,000 years ago; Watters & Fleming, 1972). This would explain the similarities between insular and continental populations and between Argentinean and Chilean populations. The time-calibrated phylogenetic reconstruction of these clades provided recently by Quintero-Galvis et al. (2021) confirmed the paleontological dating of Goin and Abello (2013) and the Miocene origin of the genus.
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The pronounced differentiation of Dromiciops north-south populations together with the important morphological differentiation observed across this range have even inspired the proposition of newDromiciops species (D’Elía, Hurtado, & D’Anatro, 2016). This idea, however, sparked an immediate debate based on species delimitation criteria, morphological comparisons, and genetic evidence (Martin, 2018; Valladares-Gómez, Celis-Diez, Palma, & Manríquez, 2017). Two subsequent studies (Suárez-Villota et al., 2018; Valladares-Gómez et al., 2019) contributed new genetic data and confirmed the existence of the “Northern” and “Southern” clusters of Dromiciops , but differentiation between these groups was not sufficient to warrant recognition as different species. Still, these studies covered a small percentage of this species large (~1200 km) geographic range. The most complete geographic sampling of Dromiciopspopulations to date was provided by Quintero-Galvis et al. (2021), who resolved genetic distances for 31 localities covering the whole geographic range for the genus. Using two mtDNA and four nuclear genes, these authors proposed four clades, being the northernmost clade different enough from the other three to be considered as a different species (Dromiciops bozinovici ). Another study by the same authors, using RAD sequencing (1856 variant SNPs), confirmed these results and proposed that the clade “C”, defined by D’Elía et al. (2016) as D. mondaca , to be redefined as a subspecies of D. gliroides (Quintero-Galvis et al., 2022).
Phenotypically, the two Dromiciops species differ mainly in the fur coloration, and the size of muzzle and ears. In general, D. bozinovici has fur that is lighter in coloration and shorter muzzle and ears than D. gliroides (see Figure 3). Behaviorally, D. bozinovici appears to have lower activity levels and reactivity to human presence and perhaps lower resting metabolism (RFN, personal observation) (Mejías et al., 2021). Both species are small (20–30 g, 110 mm snout-vent length) arboreal mammals (~30 g, 110 mm snout-vent length), with broad carnivorous-frugivorous habits (Vazquez, Rodríguez-Cabal, Gonzalez, Pacheco, & Amico, 2018; Vazquez, Zamora-Nasca, Rodriguez-Cabal, & Amico, 2021), social, sexually non-dimorphic, and are found on trees as high 30 m high in mature broadleaf forests (Godoy-Güinao, Díaz, & Celis-Diez, 2018). As with other marsupials, they accumulate fat reserves in the body and tail, which is also prehensile. Dromiciops individuals are well adapted to arboreal life; they have opposable thumbs on all four limbs, exhibiting great precision and agility when they move through the canopy. They can run vertically up the bark of the Nothofagus at speeds of up to 1 m/s and can leap with enormous precision between distant branches up to one meter far (Balazote-Oliver, Amico, Rivarola, & Morales, 2017; Mejías et al., 2021). This is attained by visual and cerebellar adaptations to discriminate distances in absolute darkness (di Virgilio, Amico, & Morales, 2014; Gurovich & Ashwell, 2020), and most likely given their Australidelphia trichromate condition (colour vision in the ultraviolet-infrared spectrum; (Arrese, Hart, Thomas, Beazley, & Shand, 2002). The recent discovery that Dromiciopsfur fluoresce pink with UV light supports this idea. This is also possible to adapt for inter-individual recognition in the dark (Y. Gurovich and R. Nespolo, personal observation). Thus, it is highly probable that Dromiciops can identify the colour of the fruits in almost complete darkness, and in turn, detect each other with visible colouration patterns in the ultraviolet zone, as in platypuses and springhares (Anich et al., 2021; Olson et al., 2021).
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