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Map of the study area along Dromiciops gliroides distribution in south-central Chile. PNVPR, Parque Nacional Vicente Pérez Rosales.
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In this study, we quantified the three pivotal genetic processes (i.e., genetic diversity, spatial genetic structuring and migration) necessary for a better biological understanding and management of the singular “living-fossil” and near-threatened mouse opossum marsupial Dromiciops gliroides, the “Monito del Monte”, in south-central Chile. We used...
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Context 1
... were collected in native forest fragments along the distributional range of D. gliroides in mainland Chile, including the northeast end of Chiloé Island (Figure 1; Table 1). Chiloé Island is located in Southern Chile between 41 and 43°S, 73 and 74°30′W, in the Los Lagos Region, and covers an area of approximately 9000 km 2 . ...
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... island represents the sole insular territory where contemporary populations of D. gliroides have been observed (Martin 2010). The northern area of the island is approximately 2.5 km from the closest point to the mainland, and it is separated by the Chacao channel (Figure 1). Animal trapping and handling were conducted following the protocol recommended by Celis- Diez et al. (2012). ...
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... program allows estimation of effective population sizes (θ = 4N e µ, where N e is the historical effective population size) and migration rates (M = m h /µ, µ is the mutation rate per generation) between population pairs based on a coalescent theory framework. We fit different migration models for 2 migration scenarios: first, a set of models to evaluate migration between the Northern and Southern clusters (see Results), and second, a set of models to evaluate migration routes between the Mainland and Chiloé Island, (Supplementary Figure 1). Within these 2 scenarios, we set 4 theoretically possible historical migration routes: 1) a Panmictic model, where the 2 populations (Northern-Southern or Mainland-Chiloé Island) were assumed to be part of the same panmictic group; 2) a one direction model, where each population has different population sizes and only migration of individuals from a particular population was allowed (from Southern to Northern cluster or from Chiloé Island to Mainland); 3) same as the previous model, but migration was allowed in the opposite direction (from Northern to Southern cluster or from Mainland to Chiloé Island; and 4) a Full model, with the 2 population sizes estimated and migration allowed to occur at different rates between the 2 populations. ...
Citations
... Previous studies have questioned the status of species of D. bozinovici, based on both genetic (Suárez-Villota et al., 2018;Valladares-Gómez et al., 2019) and morphological analyses (D'Elía et al., 2016;Martin, 2019;Valladares-Gómez et al., 2017). Our results clearly show that samples from the clade A in the north (between 35 • S to 39 • S), which were previously classified as D. bozinovici by D'Elía et al 2016, meet all the genetic criteria to be classified as distinct species. ...
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 bicinovici), 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 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 ...
... 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 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, actualized phylogeographic relationships, reproductive cycle, trophic relationships, mutualisms, conservation and threats. This marsupial shows high densities, despite presenting slow reproductive rates, a paradox that is explained by the unique characteristics of its three-dimensional habitat. We finally suggest immediate actions to protect these locally abundant but globally threatened species.
... Previously, Valladares-Gomez et al. (2019) captured one individual in RNAL for microsatellite analysis, without further descriptions (Valladares-Gomez et al. 2019). In RNAL, the forest occupies v www.esajournals.org ...
... Our phylogenetic reconstruction shows that the RNAL population associates well with the populations of the northern clade of Dromiciops, particularly with Nahuelbuta and Malleco-Tolhuaca, which is consistent with the acceptance of the Northern clade as an independent genetic unit for Dromiciops, which was elevated above the species level by D' Elia et al. (2016; D. bozinovici, which we used here; however, see discussions in Suarez-Villota et al. 2018, Valladares-Gomez et al. 2019. The existence of D. bozinovici was recently confirmed by a broad genetic-population analysis including nuclear and mitochondrial markers, and fossil calibration (J. ...
Until a few years ago, the “monito del monte” (Dromiciops gliroides) was considered the sole surviving species of Microbiotheria, the sister group of Australidelphia (Australian marsupials). However, the recent identification of a new species relegated to the northern range (Dromiciops bozinovici) and newly discovered populations of Dromiciops beyond the known limits for the geographic range demands for new studies in extreme locations. In this report, we describe the northernmost population of D. bozinovici at a high Andean location (Reserva Nacional Altos de Lircay [RNAL], which represents a record of Dromiciops distribution both in latitude [35° S] and in altitude [1696 m a.s.l.]). We live‐trapped individuals, performed behavioral observations, and extracted mtDNA (Cytb) for analyzing phylogenetic affinities. Together with confirming the phylogenetic position of RNAL within the D. bozinovici clade, interesting aspects of this isolated population arose, such as the sympatry with a didelphid marsupial (Thylamys elegans), and phylogenetic closeness with populations 300 km southward coastal. Our trapping effort yielded approximately 9.3 individuals/ha, which is relatively high compared with other small mammal populations, but typical for Dromiciops. Using in situ thermographic imaging during a night transect, we detected free‐ranging animals running vertically at ~3.6 km/h through the logs of mature trees (Nothofagus pumilio), which is fast compared with other small runners (e.g., cursorial rodents), and also compared with Dromiciops from other locations. We compared the critical time to escape, of RNAL individuals which resulted significantly higher than Dromiciops from Nahuelbuta and Valdivia, suggesting that animals from RNAL are more tolerant to human presence than other populations, which is probably due to the high level of isolation of this population. According to the IUCN the northernmost distribution of Dromiciops reaches Cauquenes, thus this report extends the distribution in 120 km to the North East. Interesting aspects, such as hibernation at freezing temperatures and the existence of a viable D. bozinovici population northward of RNAL, warrant further research on this interesting location.
... Today, Dromiciops is restricted to the temperate rainforest ("Valdivian rainforest", hereafter) (Martin, 2010), from the Maule Region (35°50'S, 72°30'W) to Chaitén (45°00'S, 72°00'W) in Chile (Oda et al., 2019), and from Neuquén Province to the Río Negro Province in Argentina (Celis-Diez et al., 2012;Gurovich et al., 2015;Martin, 2010). Although several authors have explored distinct genetic and taxonomic aspects of this group (D'Elía et al., 2016;Himes et al., 2008;Martin, 2018;Valladares-Gómez et al., 2019;, important aspects of its evolutionary history and genetic structure have yet to be fully resolved. In this context, Himes et al. (2008) evaluated Dromiciops gliroides phylogeography using two mitochondrial fragments and observed the existence of three well-differentiated clades and a marked geographic structure along the sampled range comprising Chile and Argentina. ...
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 37-48° 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.
... 200 m.a.s.l. in coastal forests to 1600 m.a.s.l. in high Andean Nothofagus pumilio ("lenga") forests (Martin, 2010;Valladares-Gómez et al., 2019). Hibernation in monitos extends from approximately May to September and animals show a marked seasonality in fat deposits and energy expenditure (Figure 3). ...
... The transition from endothermy to heterothermy is characterized by passive cooling after a sudden reduction in MR, to a limit of about 1-2 • C, when monitos start defending T b by active thermoregulation (Figure 4B). It is highly likely that monitos hibernate at freezing temperatures, since several populations in Chile and Argentina are distributed in Andean locations where temperatures go below zero in winter (Balazote-Oliver et al., 2017;Valladares-Gómez et al., 2019). During torpor in monitos, usually T b remains one or two degrees above T a , and animals could spend several weeks in this condition, where MRs are of about 5% of normothermic values, heart frequency can reach 3 beats per minute and breathing frequency could be less than 1 per minute (Nespolo et al., 2010). ...
Torpor and hibernation are powerful strategies enabling animals to survive periods of low resource availability. The state of torpor results from an active and drastic reduction of an individual’s metabolic rate (MR) associated with a relatively pronounced decrease in body temperature. To date, several forms of torpor have been described in all three mammalian subclasses, i.e., monotremes, marsupials, and placentals, as well as in a few avian orders. This review highlights some of the characteristics, from the whole organism down to cellular and molecular aspects, associated with the torpor phenotype. The first part of this review focuses on the specific metabolic adaptations of torpor, as it is used by many species from temperate zones. This notably includes the endocrine changes involved in fat- and food-storing hibernating species, explaining biomedical implications of MR depression. We further compare adaptive mechanisms occurring in opportunistic vs. seasonal heterotherms, such as tropical and sub-tropical species. Such comparisons bring new insights into the metabolic origins of hibernation among tropical species, including resistance mechanisms to oxidative stress. The second section of this review emphasizes the mechanisms enabling heterotherms to protect their key organs against potential threats, such as reactive oxygen species, associated with the torpid state. We notably address the mechanisms of cellular rehabilitation and protection during torpor and hibernation, with an emphasis on the brain, a central organ requiring protection during torpor and recovery. Also, a special focus is given to the role of an ubiquitous and readily-diffusing molecule, hydrogen sulfide (H2S), in protecting against ischemia-reperfusion damage in various organs over the torpor-arousal cycle and during the torpid state. We conclude that (i) the flexibility of torpor use as an adaptive strategy enables different heterothermic species to substantially suppress their energy needs during periods of severely reduced food availability, (ii) the torpor phenotype implies marked metabolic adaptations from the whole organism down to cellular and molecular levels, and (iii) the torpid state is associated with highly efficient rehabilitation and protective mechanisms ensuring the continuity of proper bodily functions. Comparison of mechanisms in monotremes and marsupials is warranted for understanding the origin and evolution of mammalian torpor.
... Dromiciops.-D'Elía et al. (2016a) describieron dos especies de monitos del monte, D. bozinovici y D. mondaca basado en la existencia de diferencias morfológicas cualitativas y cuantitativas entre grupos filogeográficos previamente descubiertos por Himes et al. (2008). Este esquema taxonómico ha sido cuestionado por Valladares et al. (2017Valladares et al. ( , 2019, a pesar de haber distinguido morfológicamente a D. mondaca y de no haber incluido poblaciones de esta especie en su análisis basado en microsatélites, en el que claramente se diferencia a D. bozinovici de D. gliroides. Martin (2018) un género monotípico, aun cuando sus análisis de delimitación de especies muestran que D. bozinovici representa un linaje distinto de nivel específico. ...
Se presenta una lista actualizada de los mamíferos vivientes con registros en Chile, compilada en diciembre de 2020. La lista incluye 163 especies silvestres agrupadas en 85 géneros, 31 familias y ocho órdenes. De estas especies, 20 son endémicas del país. También se provee la lista de 22 especies exóticas con poblaciones silvestres en Chile. Dado que aún persisten áreas de Chile que no han sido suficientemente exploradas, al tiempo que varios géneros no han sido adecuadamente revisados, y debido a que el estatus de algunas formas nominales es debatido, avizoramos que esta lista deberá ser actualizada en el futuro cercano.
A noticeable aspect of metatherian evolution in South America is the influence of climatic oscillations in their macroevolutionary patterns, involving major radiations during warming phases, and extinctions and functional turnovers during cooling phases. Two aspects explain why southern metatherians were more successful than their Northern Hemisphere counterparts: a well-established presence previous to the arrival of eutherians and warm climates on a continental scale. Living South American marsupials reach a maximum species richness at the edges of tropical biomes, in areas of contact between tropical and subtropical biomes, or between subtropical and temperate biomes. Three biomes concentrate 80.6% of the records of living marsupials in South America, with tropical and subtropical moist broadleaf forests including the majority of them. South American marsupials are expected to suffer great losses of suitable habitat due to climate change and land conversion. Land exploitation will continue in the immediate future, probably being more disruptive to South American biomes than the current trend in global warming. We suggest that conservation efforts focusing on stenotopic species, such as those of Caenolestidae and Microbiotheriidae, should be given high priority.
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. We present a review summarizing the recent advances on the biology of the enigmatic monito del monte, a relict Gondwanan mammal from southern South America.
Aim
Several geological events affecting Southern South America during the middle Miocene climatic optimum acted as important drivers of diversification to the biota. This is the case of Microbiotheria, for which Dromiciops is considered the sole surviving lineage, the sister group of Eomarsupialia (Australian marsupials). Three main Dromiciops genetic lineages are known, 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 (Miocenic) biogeographic history for the genus.
Location
Southern South America.
Methods
Phylogenetic reconstruction using sequences from two mitochondrial DNA and four nuclear DNA genes in 159 specimens, from 31 sites across Chile and Argentina. Divergence time estimation using fossil calibration.
Results
Our phylogenetic analysis resolved four well supported 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 would be a different species ( D. bozinovici , sensu D’elia et al. 2016). According to our estimations, this species shared a common ancestor with D. gliroides (southern clades) about 13 million years ago (95% CI: 6.4-25.3). The southern clades (39.6°S to 42.0°S), showed a divergence time ranging from 9.57 to 6.5 Mya. Strong genetic structure was detected from north to south but not across the Andes, or between Chiloé island/ mainland. Demographic equilibrium is inferred to the northern clade, and recent demographic expansions was detected in the central and southern clades.
Main conclusions
The whole diversification of Dromiciops occurred within the Miocene, being the Middle Miocene transgression (MMT), the massive marine flooding that covered several lowlands of the western face of los Andes between 38-48° S, the most likely diversifying force. This was the result of an increase in global sea levels due to the Miocene climatic optimum, which shaped the biogeographic origin of several species, including Nothofagus forests, the habitat main of Dromiciops .
