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.
<Figure 1 about here>
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.
<Figure 2 about here>
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).
<Figure 3 about here>