Dromiciops Research Articles

Local adaptation of Dromiciops marsupials (Microbiotheriidae) from southern South America: Implications for species management facing climate change.

The two species of the microbiotheriid marsupial genus Dromiciops (Dromiciops bozinovici: "Panchos's monito del monte" and Dromiciops gliroides: "monito del monte") exhibit a marked latitudinal genetic differentiation. Nevertheless, it is unclear whether this differentiation results from neutral processes or can be explained, to some extent, by local adaptation to different environmental conditions. Here, we used an SNP panel gathered by Rad-seq and searched for footprints of local adaptation (putative loci under selection) by exploring genetic associations with environmental variables in the two species of Dromiciops in Chilean and Argentinean populations. We applied three methods for detecting outlier SNPs and two genotype-environment associations approaches to quantify associations between allelic frequencies and environmental variables. Both species display strong genetic structure. D. bozinovici exhibited three distinct genetic groups, marking the first report of such structuring in this species using SNPs. In contrast, D. gliroides displayed four genetic clusters, consistent with previous studies. Both species exhibited an association of their genetic structure with environmental variables. D. bozinovici exhibited significant associations of allelic frequencies with elevation, precipitation during the warmest periods, and seasonality in the thermal regime. For D. gliroides, genetic variation appeared to be associated with more variables than D. bozinovici, including precipitation and temperature-related variables, isothermality, and elevation. All the outlier SNPs were mapped to the D. gliroides reference genome to explore if they fell within functionally known genes. These results represent a necessary first step toward identifying the genome regions that harbor genes associated with climate adaptations in Dromiciops. Notably, we identified genes involved in various functions, including carbohydrate synthesis (ALG8), muscle and neuronal regulation (MEF2D), and stress responses (PTGES3). Ultimately, this study contributes valuable insights that can inform targeted conservation strategies aimed at preserving the genetic diversity of Dromiciops in the face of environmental challenges.

The relative importance of local versus regional habitat structure variation on the abundance of two generalist mutualists along a forest disturbance gradient

Mutualistic interactions are key to biodiversity generation and maintenance, being pollination and seed dispersal interactions essential for plant reproduction. However, anthropogenic habitat disturbance can alter these interactions. We studied the regional and local effects of habitat disturbance on two generalist mutualist animals of southern Chile temperate rainforests: the hummingbird Sephanoides sephaniodes and the marsupial Dromiciops gliroides, which perform key roles as pollinator and seed disperser, respectively. We sampled 12 sites corresponding to four disturbance conditions (mature native forest, secondary forest, native forest under selective logging, and exotic forest plantations) in which we estimated the number of S. sephaniodes and D. gliroides records (as a proxy of relative abundance) using camera traps. We measured seven habitat structure variables at each site, known to influence their occurrence. Specifically, we examined S. sephaniodes and D. gliroides abundance variation at (i) a regional scale (among disturbance conditions) and (ii) at a local scale (among sampling sites). Dromiciops gliroides abundance decreased as disturbance increased, but S. sephaniodes abundance was highly variable. At the local scale, S. sephaniodes and D. gliroides abundances were largely variable among sites, influenced by habitat structural features, such as bamboo and shrub cover and woody debris. Our results show that although habitat disturbance may influence mutualist abundances, they can tolerate disturbance if minimum structure and resource requirements are met, but respond idiosyncratically to local conditions. Examining local-scale variability may provide valuable information on ecological processes, which often goes unnoticed when local sites are considered as replicates in landscape-level studies.

Climate change and population persistence in a hibernating marsupial.

Climate change has physiological consequences on organisms, ecosystems and human societies, surpassing the pace of organismal adaptation. Hibernating mammals are particularly vulnerable as winter survival is determined by short-term physiological changes triggered by temperature. In these animals, winter temperatures cannot surpass a certain threshold, above which hibernators arouse from torpor, increasing several fold their energy needs when food is unavailable. Here, we parameterized a numerical model predicting energy consumption in heterothermic species and modelled winter survival at different climate change scenarios. As a model species, we used the arboreal marsupial monito del monte (genus Dromiciops), which is recognized as one of the few South American hibernators. We modelled four climate change scenarios (from optimistic to pessimistic) based on IPCC projections, predicting that northern and coastal populations (Dromiciops bozinovici) will decline because the minimum number of cold days needed to survive the winter will not be attained. These populations are also the most affected by habitat fragmentation and changes in land use. Conversely, Andean and other highland populations, in cooler environments, are predicted to persist and thrive. Given the widespread presence of hibernating mammals around the world, models based on simple physiological parameters, such as this one, are becoming essential for predicting species responses to warming in the short term.

Effects of selective logging on genetic diversity and population structure of a keystone mistletoe

AbstractThe effects of habitat degradation remain not fully understood. A recent study reported low effects of habitat degradation on plant genetic diversity but indicates that reduction in habitat quality could impact it as well as gene flow indirectly via ecological interactions. Selective logging is a way of habitat degradation, but studies examining its effects on plant genetic diversity on non‐logged forest plant species are relatively scarce. Using 3470 single‐nucleotide polymorphisms, we assess the effects of different selective logging intensities on the genetic diversity of 66 individuals of a keystone mistletoe (Tristerix corymbosus). We also examined the possible relationship with its seed disperser (Dromiciops gliroides) abundance in three sites of the temperate rainforests of southern Chile, with different levels of selective logging intensity. Our results show that selective logging increases allelic richness and inbreeding in this mistletoe; inbreeding increased with selective logging intensity, and heterozygosity decreased with D. gliroides abundance. While wood extraction seems to positively affect T. corymbosus genetic diversity, its long‐term consequences—such as increased inbreeding—are yet to be assessed in future studies.

Modeling heterothermic fitness landscapes in a marsupial hibernator using changes in body composition.

Hibernation is an adaptive strategy that allows animals to enter a hypometabolic state, conserving energy and enhancing their fitness by surviving harsh environmental conditions. However, addressing the adaptive value of hibernation, at the individual level and in natural populations, has been challenging. Here, we applied a non-invasive technique, body composition analysis by quantitative magnetic resonance (qMR), to calculate energy savings by hibernation in a population of hibernating marsupials (Dromiciops gliroides). Using outdoor enclosures installed in a temperate rainforest, and measuring qMR periodically, we determined the amount of fat and lean mass consumed during a whole hibernation cycle. With this information, we estimated the daily energy expenditure of hibernation (DEEH) at the individual level and related to previous fat accumulation. Using model selection approaches and phenotypic selection analysis, we calculated linear (directional, β), quadratic (stabilizing or disruptive, γ) and correlational (ρ) coefficients for DEEH and fat accumulation. We found significant, negative directional selection for DEEH (βDEEH = - 0.58 ± 0.09), a positive value for fat accumulation (βFAT = 0.34 ± 0.07), and positive correlational selection between both traits (ρDEEH × FAT = 0.24 ± 0.07). Then, individuals maximizing previous fat accumulation and minimizing DEEH were promoted by selection, which is visualized by a bi-variate selection surface estimated by generalized additive models. At the comparative level, results fall within the isometric allometry known for hibernation metabolic rate in mammals. Thus, by a combination of a non-invasive technique for body composition analysis and semi-natural enclosures, we were characterized the heterothermic fitness landscape in a semi-natural population of hibernators.

Straight from the Güiñas mouth: Diet of a Neotropical carnivore documented through camera traps

Predators are known to carry prey in their mouth for many purposes, including providing for dependent young or caching. Studying predator diet through the use of remote camera traps has seldom been explored, aside from natural history observations. We provide photographic evidence of prey carrying behavior of the elusive güiñas (Leopardus guigna) in two study sites in a temperate rainforest of Chilean Patagonia. We recorded 35 photographs and 12 events of güiñas carrying prey using camera traps across 57 sites between 2019 and 2022. All photographs show a rodent as prey except in one, where based on morphology, we conclude that it is a colocolo opossum, locally known as ‘Monito del Monte’ (Dromiciops gliroides). All events happened between 2000 and 0800 h, consistent with previous research documenting diel patterns of güiñas in Chile. We argue that camera traps may offer an alternative to help us understand the feeding ecology and diet, especially when collecting scat becomes difficult (e.g., rugged terrain, sites with heavy rainfall). This work discusses the use of camera traps to study predation events and predator diets. The observations here broaden our understanding of güiña predator-prey interactions and can help generate new ways to study diet.

Torpor-responsive microRNAs in the heart of the Monito del monte, Dromiciops gliroides.

The marsupial Monito del monte (Dromiciops gliroides) utilizes both daily and seasonal bouts of torpor to preserve energy and prolong survival during periods of cold and unpredictable food availability. Torpor involves changes in cellular metabolism, including specific changes to gene expression that is coordinated in part, by the posttranscriptional gene silencing activity of microRNAs (miRNA). Previously, differential miRNA expression has been identified in D. gliroides liver and skeletal muscle; however, miRNAs in the heart of Monito del monte remained unstudied. In this study, the expression of 82 miRNAs was assessed in the hearts of active and torpid D. gliroides, finding that 14 were significantly differentially expressed during torpor. These 14 miRNAs were then used in bioinformatic analyses to identify Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways that were predicted to be most affected by these differentially expressed miRNAs. Overexpressed miRNAs were predicted to primarily regulate glycosaminoglycan biosynthesis, along with various signaling pathways such as Phosphoinositide-3-kinase/protein kinase B and transforming growth factor-β. Similarly, signaling pathways including phosphatidylinositol and Hippo were predicted to be regulated by the underexpression of miRNAs during torpor. Together, these results suggest potential molecular adaptations that protect against irreversible tissue damage and enable continued cardiac and vascular function despite hypothermia and limited organ perfusion during torpor.

Communal nesting is the optimal strategy for heat conservation in a social marsupial: lessons from biophysical models.

Endothermy, understood as the maintenance of continuous and high body temperatures owing to the combination of metabolic heat production and an insulative cover, is severely challenged in small endotherms inhabiting cold environments. As a response, social clustering combined with nest use (=communal nesting) is a common strategy for heat conservation. To quantify the actual amount of energy that is saved by this strategy, we studied the social marsupial Dromiciops gliroides (monito del monte), an endemic species of the cold forests of southern South America. It is hypothesized that sociability in this marsupial was driven by cold conditions, but evidence supporting this hypothesis is unclear. Here, we used taxidermic models ('mannequins') to experimentally test the energetic benefits of clustering combined with nest use. To do this, we fitted and compared cooling curves of solitary and grouped mannequins, within and outside of a nest, at the typical winter ambient temperatures of their habitat (5°C). We found that the strategy that minimized euthermic cost of maintenance was the combination of nest use and clustering, thus supporting communal nesting as a social adaptation to cope with the cold. Considering the basal metabolic rate of monitos, our estimates suggest that the savings represents almost half of energy consumption per day (in resting conditions). This study shows how simple biophysical models could help to evaluate bioenergetic hypotheses for social behavior in cold-adapted endotherms.

A multi-scale assessment of habitat disturbance on forest animal abundance in South American temperate rainforests

Anthropogenic disturbance has dramatically degraded and reduced the extension of the temperate rainforests of southern South America, negatively affecting forest animals that depend on habitat attributes at local and landscape scales. We conducted a multi-scale assessment (from 1 to 4000 m) to understand better how local and landscape attributes influence forest animal abundance in an anthropogenic disturbance gradient. We selected five forest-dependent animal species to assess the effects of habitat alteration: an arboreal marsupial (Dromiciops gliroides) and four forest birds (Pteroptochos tarnii, Scytalopus magellanicus, Scelorchilus rubecula, and Sylviorthorhynchus desmursii). We recorded forest animal abundances in four different habitat types (old-growth native, secondary, and logged native forests and forestry plantations). We measured local attributes in the field and characterized landscape attributes remotely. We evaluated marsupial abundance using camera traps and forest bird abundance using point counts, which were analyzed with Generalized Linear Mixed Models. Locally, canopy cover positively predicted marsupial abundance, while the number of fallen logs positively predicted bird abundance. At the landscape scale, native forest cover positively affected marsupial abundance, with significant effects at all levels. Conversely, plantation cover negatively affected forest bird abundance, while landscape heterogeneity negatively affected both groups. Our results showed that the abundance of the forest animals assessed here depends on multi-scale determinants. At the local scale, we advise greater canopy cover and maintaining woody debris. On the landscape scale, maintaining native forest cover should prioritize biodiversity management in the southern South America temperate forests. It is also crucial to control the expansion of forest plantations and reduce forest fragmentation to guarantee the persistence of forest-dependent species.

Incomplete lineage sorting and phenotypic evolution in marsupials

Incomplete lineage sorting (ILS) makes ancestral genetic polymorphisms persist during rapid speciation events, inducing incongruences between gene trees and species trees. ILS has complicated phylogenetic inference in many lineages, including hominids. However, we lack empirical evidence that ILS leads to incongruent phenotypic variation. Here, we performed phylogenomic analyses to show that the South American monito del monte is the sister lineage of all Australian marsupials, although over 31% of its genome is closer to the Diprotodontia than to other Australian groups due to ILS during ancient radiation. Pervasive conflicting phylogenetic signals across the whole genome are consistent with some of the morphological variation among extant marsupials. We detected hundreds of genes that experienced stochastic fixation during ILS, encoding the same amino acids in non-sister species. Using functional experiments, we confirm how ILS may have directly contributed to hemiplasy in morphological traits that were established during rapid marsupial speciation ca. 60 mya.

Body Composition and Energy Savings by Hibernation: Lessons from the South American Marsupial Dromiciops gliroides.

AbstractHibernation (i.e., seasonal or multiday torpor) has been described in mammals from five continents and represents an important adaptation for energy economy. However, direct quantifications of energy savings by hibernation are challenging because of the complexities of estimating energy expenditure in the field. Here, we applied quantitative magnetic resonance to determine body fat and body composition in hibernating Dromiciops gliroides (monito del monte). During an experimental period of 31 d in winter, fat was significantly reduced by g, and lean mass was significantly reduced by g. This fat and lean mass consumption is equivalent to a daily energy expenditure of hibernation (DEEH) of kJ d-1, representing 13.4% of basal metabolic rate, with a proportional contribution of fat and lean mass consumption to DEEH of 81% and 18%, respectively. During the deep heterothermic bouts of monitos, body temperature remained 0.41°C ± 0.2°C above ambient temperature, typical of hibernators. Animals shut down metabolism and passively cool down to a critical defended temperature of 5.0°C ± 0.1°C, where they begin thermoregulation in torpor. Using temperature data loggers, we obtained an empirical estimation of minimum thermal conductance of J g-1 h-1 °C-1, which is 107% of the expectation by allometric equations. With this, we parameterized body temperature/ambient temperature time series to calculate torpor parameters and metabolic rates in euthermia and torpor. Whereas the acute metabolic fall in each torpor episode is about 96%, the energy saved by hibernation is 88% (compared with the DEE of active animals), which coincides with values from the literature at similar body mass. Thus, estimating body composition provides a simple method to measure the energy saved by hibernation in mammals.

The ecology and evolution of the monito del monte, a relict species from the southern South America temperate forests.

The arboreal marsupial monito del monte (genus Dromiciops, with two recognized species) is a paradigmatic mammal. It is the sole living representative of the order Microbiotheria, the ancestor lineage of Australian marsupials. Also, this marsupial is the unique frugivorous mammal in the temperate rainforest, being the main seed disperser of several endemic plants of this ecosystem, thus acting as keystone species. Dromiciops is also one of the few hibernating mammals in South America, spending half of the year in a physiological dormancy where metabolism is reduced to 10% of normal levels. This capacity to reduce energy expenditure in winter contrasts with the enormous energy turnover rate they experience in spring and summer. The unique life history strategies of this living Microbiotheria, characterized by an alternation of life in the slow and fast lanes, putatively represent ancestral traits that permitted these cold‐adapted mammals to survive in this environment. Here, we describe the ecological role of this emblematic marsupial, summarizing the ecophysiology of hibernation and sociality, updated phylogeographic relationships, reproductive cycle, trophic relationships, mutualisms, conservation, and threats. This marsupial shows high densities, despite presenting slow reproductive rates, a paradox explained by the unique characteristics of its three‐dimensional habitat. We finally suggest immediate actions to protect these species that may be threatened in the near future due to habitat destruction and climate change.

Effects of landscape configuration on the occurrence and abundance of an arboreal marsupial from the Valdivian rainforest

BackgroundHabitat fragmentation and degradation processes affect biodiversity by reducing habitat quantity and quality, with differential effects on the resident species. However, their consequences are not always noticeable as some ecological processes affected involve idiosyncratic responses among different animal groups. The Valdivian temperate rainforests of southern Chile are experiencing a rapid fragmentation and degradation process despite being a biodiversity hotspot. Deforestation is one of the main threats to these forests. There inhabits the arboreal marsupial Dromiciops gliroides, an iconic species from the Valdivian rainforest, it is the only extant representative of the ancient Microbiotheria order, and it is currently threatened by habitat loss. Here we tested the effects of habitat configuration on D. gliroides occurrence and abundance along 12 landscapes of southern Chile with different disturbance levels.MethodsWe estimated D. gliroides occurrence and abundance using camera traps and related those metrics with landscape configuration indices obtained from FRAGSTATS (i.e., forest %, connectivity, patch number, contiguity, and distance to the nearest patch) using Bayesian linear mixed models.ResultsWe found that D. gliroides occurrence was not influenced by landscape configuration, while its abundance was positively influenced by forest contiguity.ConclusionsAlthough this arboreal marsupial is present in disturbed forests, its restricted movement capabilities and high dependency on the forest three-dimensional structure may affect its long-term persistence. We urge to rethink native forest conservation and management policies to improve habitat connectivity with possible positive consequences for native fauna.

Geographical context outweighs habitat disturbance effects in explaining mistletoe population genetic differentiation at a regional scale.

Genetic differentiation depends on ecological and evolutionary processes that operate at different spatial and temporal scales. While the geographical context is likely to determine large-scale genetic variation patterns, habitat disturbance events will probably influence small-scale genetic diversity and gene flow patterns. Therefore, the genetic diversity patterns that we observe today result from the combination of both processes, but they are rarely assessed simultaneously. We determined the population structure and genetic diversity of a hemiparasitic mistletoe (Tristerix corymbosus) from the temperate rainforests of southern Chile to determine the effects of geographical context and habitat disturbance at a regional scale and if it is affected by the abundance and occurrence of its seed disperser mutualist (the arboreal marsupial Dromiciops gliroides). We genotyped 359 individuals from 12 populations using single nucleotide polymorphisms, across three different geographical contexts and four disturbance conditions. We also used camera traps to estimate the abundance and occurrence of the seed disperser. Our results suggest that genetic differences among populations are related more to geographical context than to habitat disturbance. However, as disturbance increased, D.gliroides abundance and occurrence decreased, and mistletoe inbreeding index (FIS ) increased. We also found highly uneven gene flow among study sites. Despite the high levels of disturbance that these temperate rainforests are facing, our results suggest that mistletoe genetic differentiation at a regional scale was more influenced by historical events. However, habitat disturbance can indirectly affect mistletoe population genetic differentiation via the seed dispersal process, which may increase levels of inbreeding.

Genomic diversity and demographic history of the Dromiciops genus (Marsupialia: Microbiotheriidae)

Three orders represent the South American fauna of marsupials. Of these, Microbiotheria was until recently known as a monotypic genus with the only surviving species Dromiciops gliroides (monito del monte). The recent proposal of a new Dromiciops species (Dromiciops bozinovici), together with new information on the origin and diversification of living microbioterians has changed the prevailing paradigm around the evolutionary history of these emblematic marsupials. Here, we used a RADseq approach to test for evidence of admixture and past or current gene flow among both species of Dromiciops and evaluate the genetic structure within D. gliroides. We analyzed 127 samples of Dromiciops distributed across the known distribution range of both species. We also inferred the joint demographic history of these lineages, thus corroborating the status of D. bozinovici as a distinct species. Demographic history reconstruction indicated that D. bozinovici diverged from D. gliroides around 4my ago and has remained isolated and demographically stable ever since. In contrast, D. gliroides is subdivided into three subclades that experienced recent expansions and moderate gene flow among them (mostly from north to south). Furthermore, genetic distances among populations within D. gliroides were significantly correlated with geographic distances. These results suggest that some of the D. gliroides populations would have survived in glacial refuges, with posterior expansions after ice retreat. Our results have important implications for the systematics of the genus and have profound conservation consequences for the new species, especially considering the fragmentation level of the temperate rainforest.

The forest gardener: A marsupial with a key seed‐dispersing role in the Patagonian temperate forest

AbstractSeed dispersal by vertebrate animals is critical for the establishment of fleshy‐fruited plant species. In regions with impoverished faunas, such as the Patagonian temperate forest, the arboreal marsupial Dromiciops gliroides plays a key role as a seed disperser. Here, we assessed the ecological role of D. gliroides as a seed disperser and their possible effects on the plant structure of the Patagonian temperate forest. We found that the passage through the digestive tract of D. gliroides increased germination rate in four of the five groups of plants evaluated. Additionally, we found that D. gliroides disperses all the epiphytes, almost a quarter of the vines and parasites, and could disperse about half of the trees and shrubs present in the Patagonian temperate forest. Taken together, our results demonstrate the keystone dispersing role played by D. gliroides within the Patagonian temperate forest and highlight the importance of its conservation for the preservation of this highly endemic flora.

A Mesocosm Experiment in Ecological Physiology: The Modulation of Energy Budget in a Hibernating Marsupial under Chronic Caloric Restriction.

AbstractDuring the past 60 years, mammalian hibernation (i.e., seasonal torpor) has been interpreted as a physiological adaptation for energy economy. However, direct field comparisons of energy expenditure and torpor use in hibernating and active free-ranging animals are scarce. Here, we followed the complete hibernation cycle of a fat-storing hibernator, the marsupial Dromiciops gliroides, in its natural habitat. Using replicated mesocosms, we experimentally manipulated energy availability and measured torpor use, hibernacula use, and social clustering throughout the entire hibernation season. Also, we measured energy flow using daily food intake, daily energy expenditure (DEE), and basal metabolic rate (BMR) in winter. We hypothesized that when facing chronic caloric restriction (CCR), a hibernator should maximize torpor frequency to compensate for the energetic deficit, compared with individuals fed ad lib. (controls). However, being torpid at low temperatures could increase other burdens (e.g., cost of rewarming, freezing risks). Our results revealed that CCR animals, compared with control animals, did not promote heat conservation strategies (i.e., clustering and hibernacula use). Instead, they gradually increased torpor frequency and reduced DEE and, as a consequence, recovered weight at the end of the season. Also, CCR animals consumed food at a rate of 50.8 kJ d-1, whereas control animals consumed food at a rate of 98.4 kJ d-1. Similarly, the DEE of CCR animals in winter was kJ d-1, which was significantly lower than control animals ( kJ d-1). However, BMR and lean mass of CCR and control animals did not vary significantly, suggesting that animals maintained full metabolic capacities. This study shows that the use of torpor can be modulated depending on energy supply, thus optimizing energy budgeting. This plasticity in the use of heterothermy as an energy-saving strategy would explain the occurrence of this marsupial in a broad latitudinal and altitudinal range. Overall, this study suggests that hibernation is a powerful strategy to modulate energy expenditure in mammals from temperate regions.

Intermediate levels of wood extraction may facilitate coexistence of an endemic arboreal marsupial and Indigenous communities

AbstractLand-use change is a major driver of biodiversity loss. Large-scale disturbances such as habitat loss, fragmentation and degradation are known to have negative consequences for native biota, but the effects of small-scale disturbances such as selective logging are less well known. We compared three sites with different regimes of selective logging performed by Indigenous communities in the South American temperate rainforest, to assess effects on the density and habitat selection patterns of the Near Threatened endemic arboreal marsupial Dromiciops gliroides. We used structured interviews to identify patterns of wood extraction, which was 0.22–2.55 m3 per ha per year. In the less disturbed site only two tree species were logged, in the intermediately disturbed sites eight species were logged at low intensity, and in the most disturbed site seven species were logged intensively. The site with intermediate disturbance had the highest fleshy-fruited plant diversity and fruit biomass values as a result of the proliferation of shade-intolerant plants. This site also had the highest density of D. gliroides. These findings are consistent with Connell's intermediate disturbance hypothesis, suggesting that coexistence of people with nature is possible if wood extraction volumes are moderate, increasing plant diversity. Indigenous communities have sustainably used natural resources for centuries, but current rates of land-use change are becoming a significant threat to both them and their natural resources.

Heterothermy as the Norm, Homeothermy as the Exception: Variable Torpor Patterns in the South American Marsupial Monito del Monte (Dromiciops gliroides).

Hibernation (i.e., multiday torpor) is considered an adaptive strategy of mammals to face seasonal environmental challenges such as food, cold, and/or water shortage. It has been considered functionally different from daily torpor, a physiological strategy to cope with unpredictable environments. However, recent studies have shown large variability in patterns of hibernation and daily torpor (“heterothermic responses”), especially in species from tropical and subtropical regions. The arboreal marsupial “monito del monte” (Dromiciops gliroides) is the last living representative of the order Microbiotheria and is known to express both short torpor episodes and also multiday torpor depending on environmental conditions. However, only limited laboratory experiments have documented these patterns in D. gliroides. Here, we combined laboratory and field experiments to characterize the heterothermic responses in this marsupial at extreme temperatures. We used intraperitoneal data loggers and simultaneous measurement of ambient and body temperatures (TA and TB, respectively) for analyzing variations in the thermal differential, in active and torpid animals. We also explored how this differential was affected by environmental variables (TA, natural photoperiod changes, food availability, and body mass changes), using mixed-effects generalized linear models. Our results suggest that: (1) individuals express short bouts of torpor, independently of TA and even during the reproductive period; (2) seasonal torpor also occurs in D. gliroides, with a maximum bout duration of 5 days and a mean defended TB of 3.6 ± 0.9°C (one individual controlled TB at 0.09°C, at sub-freezing TA); (3) the best model explaining torpor occurrence (Akaike information criteria weight = 0.59) discarded all predictor variables except for photoperiod and a photoperiod by food interaction. Altogether, these results confirm that this marsupial expresses a dynamic form of torpor that progresses from short torpor to hibernation as daylength shortens. These data add to a growing body of evidence characterizing tropical and sub-tropical heterothermy as a form of opportunistic torpor, expressed as daily or seasonal torpor depending on environmental conditions.

The biogeography of Dromiciops in southern South America: Middle Miocene transgressions, speciation and associations with Nothofagus

The current distribution of the flora and fauna of southern South America is the result of drastic geological events that occurred during the last 20 million years, including marine transgressions, glaciations and active vulcanism. All these have been associated with fragmentation, isolation and subsequent expansion of the biota, south of 35°S, such as the temperate rainforest. This forest is mostly dominated by Nothofagus trees and is the habitat of the relict marsupial monito del monte, genus Dromiciops, sole survivor of the order Microbiotheria. Preliminary analyses using mtDNA proposed the existence of three main Dromiciops lineages, distributed latitudinally, whose divergence was initially attributed to recent Pleistocene glaciations. Using fossil-calibrated dating on nuclear and mitochondrial genes, here we reevaluate this hypothesis and report an older (Miocene) biogeographic history for the genus. We performed phylogenetic reconstructions using sequences from two mitochondrial DNA and four nuclear DNA genes in 159 specimens from 31 sites across Chile and Argentina. Our phylogenetic analysis resolved three main clades with discrete geographic distributions. The oldest and most differentiated clade corresponds to that of the northern distribution (35.2°S to 39.3°S), which should be considered a distinct species (D. bozinovici, sensu D’Elía et al. 2016). According to our estimations, this species shared a common ancestor with D. gliroides (southern clades) about ~13 million years ago. Divergence time estimates for the southern clades (39.6°S to 42.0°S) ranged from 9.57 to 6.5 Mya. A strong genetic structure was also detected within and between clades. Demographic analyses suggest population size stability for the northern clade (D. bozinovici), and recent demographic expansions for the central and southern clades. All together, our results suggest that the diversification of Dromiciops were initiated by the Middle Miocene transgression (MMT), the massive marine flooding that covered several lowlands of the western face of Los Andes between 37 and 48°S. The MMT resulted from an increase in global sea levels at the Miocene climatic optimum, which shaped the biogeographic origin of several species, including Nothofagus forests, the habitat of Dromiciops.