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.

Hepatozoon (Eucoccidiorida: Hepatozoidae) in wild mammals of the Americas: a systematic review.

BACKGROUND: The study of parasites provides insight into intricate ecological relationships in ecosystem dynamics, food web structures, and evolution on multiple scales. Hepatozoon Eucoccidiorida: Hepatozoidae) is a genus of protozoan hemoparasites with heteroxenous life cycles that switch infections between vertebrates and blood-feeding invertebrates. The most comprehensive review of the genus was published 26 years ago, and currently there are no harmonized data on the epizootiology, diagnostics, genotyping methods, evolutionary relationships, and genetic diversity of Hepatozoon in the Americas. METHODS: Here, we provide a comprehensive review based on the PRISMA method regarding Hepatozoon in wild mammals within the American continent, in order to generate a framework for future research. RESULTS: 11 out of the 35 countries of the Americas (31.4%) had data on Hepatozoon, with Carnivora and Rodentia orders having the most characterizations. Bats, ungulates, and shrews were the least affected groups. While Hepatozoon americanum, H. americanum-like, H. canis, H. didelphydis, H. felis, H. milleri, H. griseisciuri, and H. procyonis correspond to the identified species, a plethora of genospecies is pending for a formal description combining morphology and genetics. Most of the vectors of Hepatozoon in the Americas are unknown, but some flea, mite, and tick species have been confirmed. The detection of Hepatozoon has relied mostly on conventional polymerase chain reaction (PCR), and the implementation of specific real time PCR for the genus needs to be employed to improve its diagnosis in wild animals in the future. From a genetic perspective, the V4 region of the 18S rRNA gene has been widely sequenced for the identification of Hepatozoon in wild animals. However, mitochondrial and apicoplast markers should also be targeted to truly determine different species in the genus. A phylogenetic analysis of herein retrieved 18S ribosomal DNA (rDNA) sequences showed two main clades of Hepatozoon: Clade I associated with small mammals, birds, and herpetozoa, and Clade II associated with Carnivora. The topology of the tree is also reflected in the haplotype network. CONCLUSIONS: Finally, our review emphasizes Hepatozoon as a potential disease agent in threatened wild mammals and the role of wild canids as spreaders of Hepatozoon infections in the Americas.

A Comparative Phylogeography of Three Marine Species with Different PLD Modes Reveals Two Genetic Breaks across the Southern Caribbean Sea.

The comparative phylogeography of marine species with contrasting dispersal potential across the southern Caribbean Sea was evaluated by the presence of two putative barriers: the Magdalena River plume (MRP) and the combination of the absence of a rocky bottom and the almost permanent upwelling in the La Guajira Peninsula (ARB + PUG). Three species with varying biological and ecological characteristics (i.e., dispersal potentials) that inhabit shallow rocky bottoms were selected: Cittarium pica (PLD < 6 days), Acanthemblemaria rivasi (PLD < 22 days), and Nerita tessellata (PLD > 60 days). We generated a set of SNPs for the three species using the ddRad-seq technique. Samples of each species were collected in five locations from Capurganá to La Guajira. For the first time, evidence of a phylogeographic break caused by the MRP is provided, mainly for A. rivasi (AMOVA: ΦCT = 0.420). The ARB + PUG barrier causes another break for A. rivasi (ΦCT = 0.406) and C. pica (ΦCT = 0.224). Three populations (K = 3) were identified for A. rivasi and C. pica, while N. tessellata presented one population (K = 1). The Mantel correlogram indicated that A. rivasi and C. pica fit the hierarchical population model, and only the A. rivasi and C. pica comparisons showed phylogeographic congruence. Our results demonstrate how the biological traits of these three species and the biogeographic barriers have influenced their phylogeographic structure.

Late Pleistocene-dated divergence between South Hemisphere populations of the non-conventional yeast L. cidri.

Most organisms belonging to the Saccharomycotina subphylum have high genetic diversity and a vast repertoire of metabolisms and lifestyles. Lachancea cidri is an ideal yeast model for exploring the interplay between genetics, ecological function and evolution. Lachancea cidri diverged from the Saccharomyces lineage before the whole-genome duplication and is distributed across the South Hemisphere, displaying an important ecological success. We applied phylogenomics to investigate the genetic variation of L. cidri isolates obtained from Australia and South America. Our approach revealed the presence of two main lineages according to their geographic distribution (Aus and SoAm). Estimation of the divergence time suggests that SoAm and Aus lineages diverged near the last glacial maximum event during the Pleistocene (64-8 KYA). Interestingly, we found that the French reference strain is closely related to the Australian strains, with a recent divergence (405-51 YA), likely associated to human movements. Additionally, we identified different lineages within the South American population, revealing that Patagonia contains a similar genetic diversity comparable to that of other lineages in S. cerevisiae. These findings support the idea of a Pleistocene-dated divergence between South Hemisphere lineages, where the Nothofagus and Araucaria ecological niches likely favoured the extensive distribution of L. cidri in Patagonia.

Apicomplexans in small mammals from Chile, with the first report of the Babesia microti group in South American rodents.

Small mammals play an essential role as disseminators of pathogens because they reach high population densities and have ubiquitous distributions. In the Northern Hemisphere rodents are well recognized as reservoirs for tick-borne bacteria of the Anaplasmataceae family and also apicomplexan protozoans. In contrast, South American rodents hosting these microorganisms have been rarely identified. In this study, we collected blood from rodents and marsupials in northern Chile and screened for Anaplasmataceae bacteria and apicomplexan protozoa. Overall, 14.7% of the samples were positive for Babesia, Hepatozoon, and Sarcocystidae using conventional PCR assays targeting the structural 18S rRNA locus (18S). Phylogenetic analyses performed with amplicons derived from 18S and cytochrome c oxidase (COI) gene provided evidence of a Babesia sp. belonging to the Babesia microti group in Phyllotis darwini, and a novel Babesia genotype in P. darwini and Abrothrix jelskii. Furthermore, four novel genotypes of Hepatozoon retrieved from Abrothrix olivacea, P. darwini, and Oligoryzomys longicaudatus, formed independent lineages within a clade that includes additional Hepatozoon spp. detected in South American rodents. Moreover, an incidental finding of a previously detected apicomplexan, herein designated as Sarcocystidae sp., was recorded in Thylamys opossums with a high prevalence, indicating a possible specific association with these mammals. Phylogenetic analysis of Sarcoystidae sp. clearly demonstrated its relatedness to apicomplexans detected in Australian marsupials. Our results expand the range of mammals hosting tick-borne apicomplexans in South America, highlight a novel clade consisting of South American babesias, and report for the first time the B. microti group infecting rodents in the region.

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 (T A and T B, respectively) for analyzing variations in the thermal differential, in active and torpid animals. We also explored how this differential was affected by environmental variables (T A, 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 T A 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 T B of 3.6 ± 0.9°C (one individual controlled T B at 0.09°C, at sub-freezing T A); (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.

Baja variabilidad y diferenciación genética poblacional en la "lisa", Mugil incilis (Teleostei: Mugilidae) del Caribe colombiano

La "Lisa" Mugil incilis, es uno de los recursos ícticos más importante de la industria pesquera artesanal del Caribe de Colombia. Sin embargo, sus poblaciones llevan siendo sobreexplotadas por décadas, que en conjunto con el deterioro de su hábitat podrían estar causando un efecto negativo en la variabilidad genética de las mismas. Con el objetivo de generar información científica que permita apoyar decisiones y políticas más adecuadas de manejo pesquero y conservación se evaluó la variabilidad y la estructura genética de M. incilis a lo largo de la costa del Caribe de Colombia. Se seleccionaron seis sistemas costeros, entre ellos tres lagunas costeras de acceso abierto a la pesca (Ciénaga La Virgen, Ciénaga La Caimanera y Bahía de Cispatá) y tres santuarios de fauna y flora de la red de Parques Nacionales Naturales de Colombia (los santuarios de fauna y flora Los Flamencos, Ciénaga Grande de Santa Marta y El Corchal). Se utilizaron siete loci microsatélites, los cuales revelaron 94 alelos con un promedio de 11.6 alelos por locus. Los valores de variabilidad genética en todos los sitios de muestreo fueron bajos (Ho = 0.108-0.402), aunque demostraron tener un alto potencial genético (He = 0.772-0.868). Se encontró que todos los loci presentaron desequilibrio de Hardy-Weinberg debido a una deficiencia de heterocigotos. Esto fue concordante con los eventos de cuellos de botellas recientes que se determinaron en todas las lagunas y las causas pueden ser la sobrepesca y la presencia de alelos nulos. Los resultados del análisis de estructuración genética demostraron la existencia de tres poblaciones, una conformada por las localidades ubicadas desde el sector de La Guajira hasta Sucre y una segunda en Bahía de Cispatá y la tercera en la Ciénaga La Caimanera. Este estudio sugiere que los procesos involucrados en el nivel de aprovechamiento pesquero, en el ciclo reproductivo y en las condiciones oceanográficas de la región del Caribe Sur determinan la variabilidad y estructura genética de M. incilis. Se proponen recomendaciones para el manejo y conservación de M. incilis.

The "Mullet" Mugil incilis is one of the most important fish resources of the artisanal fishing industry of the Colombian Caribbean. However, their populations are being overexploited for decades, which together with the deterioration of their habitat could be causing a negative effect on the genetic variability of their populations. In order to generate scientific information to support decisions and more appropriate fisheries management and conservation policies, the variability and genetic structure of M. incilis along the Caribbean coast of Colombia was evaluated. Six coastal systems were selected, including three coastal lagoon systems with open access to fishing (Ciénaga La Virgen, Ciénaga La Caimanera and Bahía de Cispatá) and three coastal lagoons belonging to fauna and flora sanctuaries of the network of National Natural Parks of Colombia (Los Flamencos, Ciénaga Grande de Santa Marta and El Corchal). Seven microsatellite loci were used, which revealed 94 alleles with an average of 11.6 alleles per locus. The values of genetic variability in all sampling sites were low (Ho = 0.108-0.402), although they showed a high genetic potential (He = 0.772-0.868). All the loci presented departures from the Hardy-Weinberg expectations due to a deficiency of heterozygotes. This was in agreement with the events of recent bottlenecks that were determined in all the lagoons and the causes could be overfishing and the presence of null alleles. The analysis of genetic structuring revealed the existence of two populations, one formed by the localities located from La Guajira to Sucre; a second in Bahía de Cispatá and the third one in Ciénaga La Caimanera. This study suggests that the processes involved in the level of fishing exploitation, in the reproductive cycle and in the oceanographic conditions of the South Caribbean region determine the genetic variability and structure of M. incilis. Recommendations for the management and conservation of M. incilis are proposed.

A functional transcriptomic analysis in the relict marsupial Dromiciops gliroides reveals adaptive regulation of protective functions during hibernation.

The small South American marsupial, Dromiciops gliroides, known as the missing link between the American and the Australian marsupials, is one of the few South American mammals known to hibernate. Expressing both daily torpor and seasonal hibernation, this species may provide crucial information about the mechanisms and the evolutionary origins of marsupial hibernation. Here, we compared torpid and active individuals, applying high-throughput sequencing technologies (RNA-seq) to profile gene expression in three D. gliroides tissues and determine whether hibernation induces tissue-specific differential gene expression. We found 566 transcripts that were significantly up-regulated during hibernation (369 in brain, 147 in liver and 50 in skeletal muscle) and 339 that were down-regulated (225 in brain, 79 in liver and 35 in muscle). The proteins encoded by these differentially expressed genes orchestrate multiple metabolic changes during hibernation, such as inhibition of angiogenesis, prevention of muscle disuse atrophy, fuel switch from carbohydrate to lipid metabolism, protection against reactive oxygen species and repair of damaged DNA. According to the global enrichment analysis, brain cells seem to differentially regulate a complex array of biological functions (e.g., cold sensitivity, circadian perception, stress response), whereas liver and muscle cells prioritize fuel switch and heat production for rewarming. Interestingly, transcripts of thioredoxin-interacting protein (TXNIP), a potent antioxidant, were significantly over-expressed during torpor in all three tissues. These results suggest that marsupial hibernation is a controlled process where selected metabolic pathways show adaptive modulation that can help to maintain homeostasis and enhance cytoprotection in the hypometabolic state.

Mitogenomics of southern hemisphere blue mussels (Bivalvia: Pteriomorphia): Insights into the evolutionary characteristics of the Mytilus edulis complex.

Marine blue mussels (Mytilus spp.) are widespread species that exhibit an antitropical distribution with five species occurring in the Northern Hemisphere (M. trossulus, M. edulis, M. galloprovincialis, M. californianus and M. coruscus) and three in the Southern Hemisphere (M. galloprovincialis, M. chilensis and M. platensis). Species limits in this group remain controversial, in particular for those forms that live in South America. Here we investigated structural characteristics of marine mussels mitogenomes, based on published F mtDNA sequences of Northern Hemisphere species and two newly sequenced South American genomes, one from the Atlantic M. platensis and another from the Pacific M. chilensis. These mitogenomes exhibited similar architecture to those of other genomes of Mytilus, including the presence of the Atp8 gene, which is missing in most of the other bivalves. Our evolutionary analysis of mitochondrial genes indicates that purifying selection is the predominant force shaping the evolution of the coding genes. Results of our phylogenetic analyses supported the monophyly of Pteriomorphia and fully resolved the phylogenetic relationships among its five orders. Finally, the low genetic divergence of specimens assigned to M. chilensis and M. platensis suggests that these South American marine mussels represent conspecific variants rather than distinct species.

Molecular phyloeeny of the neritidae (gastropod: neritimorpha) based on the miitochondrial genes cytochrome oxidase i (coi) and 16s rrna / Filogenia molecular de la familia Neritidae (Gastropoda: Neritimorpha) con base en los genes mitocondriales citocromo oxidasa I (COI) y 16S rRNA

The family Neritidae has representatives in tropical and subtropical regions that occur in a variety of environments, and its known fossil record dates back to the late Cretaceous. However there have been few studies of molecular phylogeny in this family. We performed a phylogenetic reconstruction of the family Neritidae using the COI (722 bp) and the 16S rRNA (559 bp) regions of the mitochondrial genome. Neighbor-joining, maximum parsimony and Bayesian inference were performed. The best phylogenetic reconstruction was obtained using the COI region, and we consider it an appropriate marker for phylogenetic studies within the group. Consensus analysis (COI +16S rRNA) generally obtained the same tree topologies and confirmed that the genus Nerita is monophyletic. The consensus analysis using parsimony recovered a monophyletic group consisting of the genera Neritina, Septaria, Theodoxus, Puperita, and Clithon, while in the Bayesian analyses Theodoxus is separated from the other genera. The phylogenetic status of the species from the genus Nerita from the Colombian Caribbean generated in this study was consistent with that reported for the genus in previous studies. In the resulting consensus tree obtained using maximum parsimony, we included information on habitat type for each species, to map the evolution by habitat. Species of the family Neritidae possibly have their origin in marine environments, which is consistent with conclusions from previous reports based on anatomical studies.

La familia Neritidae cuenta con representantes en regiones tropicales y subtropicales adaptadas a diferentes ambientes, con un registro fósil que data para finales del Cretáceo. Sin embargo no se han realizado estudios de filogenia molecular en la familia. En este estudio se realizó una reconstrucción filogenética de la familia Neritidae utilizando las regiones COI (722 pb) y 16S rRNA (559 pb) del genoma mitocondrial. Se realizaron análisis de distancias de Neighbor-Joining, Máxima Parsimonia e Inferencia Bayesiana. La mejor reconstrucción filogenética fue mediante la región COI, considerándola un marcador apropiado para realizar estudios filogenéticos dentro del grupo. El consenso de las relaciones filogenéticas (COI+16S rRNA) permitió confirmar que el género Nerita es monofilético. El consenso del análisis de parsimonia reveló un grupo monofilético formado por los géneros Neritina, Septaria, Theodoxus, Puperita y Clithon, mientras que en el análisis bayesiano Theodoxus se encuentra separado de los otros géneros. El resultado en las especies del género Nerita del Caribe colombiano fue consistente con lo reportado para el género en estudios previos. En el árbol resultante del análisis de parsimonia se sobrepuso la información del hábitat de cada especie, para mapear la evolución por hábitat. Se obtuvo como resultado que las especies de la familia Neritidae posiblemente tengan su origen en un ambiente marino, siendo congruente con lo reportado en estudios anatómicos realizados anteriormente.