Mammalian Strategies Research Articles

Adapting to stress: The effects of hibernation and hibernacula temperature on the hepatic transcriptome of Rhinolophus pusillus.

Hibernation, a survival strategy in mammals for extreme climates, induces physiological phenomena such as ischemia-reperfusion and metabolic shifts that hold great potential for advancements in modern medicine. Despite this, the molecular mechanisms underpinning hibernation remain largely unclear. This study used RNA-seq and Iso-seq techniques to investigate the changes in liver transcriptome expression of Rhinolophus pusillus during hibernation and active periods, as well as under different microhabitat temperatures. We identified 11 457 differentially expressed genes during hibernation and active periods, of which 395 showed significant differential expression. Genes associated with fatty acid catabolism were significantly upregulated during hibernation, whereas genes related to carbohydrate metabolism and glycogen synthesis were downregulated. Conversely, immune-related genes displayed differential expression patterns: genes tied to innate immunity were significantly upregulated, while those linked to adaptive immunity and inflammatory response were downregulated. The analysis of transcriptomic data obtained from different microhabitat temperatures revealed that R. pusillus exhibited an upregulation of genes associated with lipid metabolism in lower microhabitat temperature. This upregulation facilitated an enhanced utilization rate of triglyceride, ultimately resulting in increased energy provision for the organism. Additionally, R. pusillus upregulated gluconeogenesis-related genes regardless of the microhabitat temperature, demonstrating the importance of maintaining blood glucose levels during hibernation. Our transcriptomic data reveal that these changes in liver gene expression optimize energy allocation during hibernation, suggesting that liver tissue adaptively responds to the inherent stress of its function during hibernation. This study sheds light on the role of differential gene expression in promoting more efficient energy allocation during hibernation. It contributes to our understanding of how liver tissue adapts to the stressors associated with this state.

Black-and-white pelage as visually protective coloration in colobus monkeys

Conspicuous coloration is often seen as the evolutionary consequence of either sexual selection or warning predators visually about prey defences, although not all conspicuous species fit this paradigm. Exceptions include several species of colobus monkeys whose black-and-white coloration, characteristic of larger colobines, has never been explained. Here, using photographs of black-and-white colobus (Colobus vellerosus) taken in the wild, quantitative image analysis, and vision modelling (acuity-corrected feline, chimpanzee, and raptor vision), we provide evidence that their coloration provides distance-dependent camouflage in natural forest environments. At all viewing distances, black-and-white colobus monkeys blend into their environment because of their high chromatic overlap with the background when viewed by ecologically relevant predator vision models which have low visual acuities. Additionally, for chimpanzee and felid vision, there was evidence of edge disruption at longer viewing distances. Our comparative analyses of different species of colobines do not support an association between black-and-white coloration and larger body mass or group size, but this may simply be due to the limited number of species within the family. We reason that black-and-white colobines gain visually protective coloration through background matching against felids, and also benefit through disruptive coloration against felids and chimpanzees but rely on these protective coloration mechanisms less against raptors.Significance statementConspicuous black-and-white coloration in colobus monkeys has long eluded an evolutionary explanation. Our research, employing photographs of colobus monkeys, image analysis, and vision modelling, unveils a novel approach to this coloration. We show that in their natural forest habitats, black-and-white colobus monkeys employ distance-dependent camouflage against ecologically relevant predators with low visual acuity, blending in with the background at increasing viewing distances. In summary, the evolution of black-and-white colobus coloration appears to be related to background matching against felids, with added benefits of disruptive camouflage against felids and chimpanzees, less so to raptors, offering fresh insights into the complex interplay of coloration and survival strategies in mammals.

Trabecular bone morphology in big cats reflects the complex diversity of limb use but not home range size or daily travel distance.

A relationship exists between mechanical loading and bone morphology. Although studies show a relationship between trabecular bone morphology and locomotor strategy in mammals, none of them have studied trabecular bone morphology in felid species occupying disparate and overlapping habitats. We investigate trabecular bone volume fraction (BVF) in the femoral and humeral heads, and distal tibia of four felid species (mountain lions, jaguars, cheetahs, and leopards) to identify whether there is a relationship between BVF and locomotor behavior. This study's goals are to identify whether felid species with high daily travel distance or large home range size have greater BVF compared with those with small daily travel distance or home range size, and whether BVF is correlated among the three elements of the fore and hindlimb studied. We quantified BVF in micro- and peripheral computed tomography images and found no significant differences across species in the femoral and humeral head (p > 0.05). However, in the distal tibia, results showed that leopards, mountain lions, and cheetahs have significantly greater (p < 0.05) BVF than jaguars. Despite differences in home range size and daily travel distance, the proximal elements did not reflect differences in BVF; however, the distal-most element did, suggesting decreased loading among jaguars. These findings suggest that the observed pattern of trabecular bone morphology is potentially due to the diversity in locomotor strategy of the forelimb. Additionally, these results imply that neither home range size nor daily travel distance are clear indicators of activity levels. A cautious approach is warranted in studying how loading influences trabecular morphology.

Nitrogen recycling via gut symbionts increases in ground squirrels over the hibernation season.

Hibernation is a mammalian strategy that uses metabolic plasticity to reduce energy demands and enable long-term fasting. Fasting mitigates winter food scarcity but eliminates dietary nitrogen, jeopardizing body protein balance. Here, we reveal gut microbiome-mediated urea nitrogen recycling in hibernating thirteen-lined ground squirrels (Ictidomys tridecemlineatus). Ureolytic gut microbes incorporate urea nitrogen into metabolites that are absorbed by the host, with the nitrogen reincorporated into the squirrel's protein pool. Urea nitrogen recycling is greatest after prolonged fasting in late winter, when urea transporter abundance in gut tissue and urease gene abundance in the microbiome are highest. These results reveal a functional role for the gut microbiome during hibernation and suggest mechanisms by which urea nitrogen recycling may contribute to protein balance in other monogastric animals.

A chromosome-level genome of Antechinus flavipes provides a reference for an Australian marsupial genus with male death after mating.

The 15 species of small carnivorous marsupials that comprise the genus Antechinus exhibit semelparity, a rare life‐history strategy in mammals where synchronized death occurs after one breeding season. Antechinus males, but not females, age rapidly (demonstrate organismal senescence) during the breeding season and show promise as new animal models of ageing. Some antechinus species are also threatened or endangered. Here, we report a chromosome‐level genome of a male yellow‐footed antechinus Antechinus flavipes. The genome assembly has a total length of 3.2 Gb with a contig N50 of 51.8 Mb and a scaffold N50 of 636.7 Mb. We anchored and oriented 99.7% of the assembly on seven pseudochromosomes and found that repetitive DNA sequences occupy 51.8% of the genome. Draft genome assemblies of three related species in the subfamily Phascogalinae, two additional antechinus species (Antechinus argentus and A. arktos) and the iteroparous sister species Murexia melanurus, were also generated. Preliminary demographic analysis supports the hypothesis that climate change during the Pleistocene isolated species in Phascogalinae and shaped their population size. A transcriptomic profile across the A. flavipes breeding season allowed us to identify genes associated with aspects of the male die‐off. The chromosome‐level A. flavipes genome provides a steppingstone to understanding an enigmatic life‐history strategy and a resource to assist the conservation of antechinuses.

Appendage Regeneration in Vertebrates: What Makes This Possible?

The ability to regenerate amputated or injured tissues and organs is a fascinating property shared by several invertebrates and, interestingly, some vertebrates. The mechanism of evolutionary loss of regeneration in mammals is not understood, yet from the biomedical and clinical point of view, it would be very beneficial to be able, at least partially, to restore that capability. The current availability of new experimental tools, facilitating the comparative study of models with high regenerative ability, provides a powerful instrument to unveil what is needed for a successful regeneration. The present review provides an updated overview of multiple aspects of appendage regeneration in three vertebrates: lizard, salamander, and zebrafish. The deep investigation of this process points to common mechanisms, including the relevance of Wnt/β-catenin and FGF signaling for the restoration of a functional appendage. We discuss the formation and cellular origin of the blastema and the identification of epigenetic and cellular changes and molecular pathways shared by vertebrates capable of regeneration. Understanding the similarities, being aware of the differences of the processes, during lizard, salamander, and zebrafish regeneration can provide a useful guide for supporting effective regenerative strategies in mammals.

Evaluating tooth strontium and barium as indicators of weaning age in Pacific walruses.

Lactation length and weaning age provide important information about maternal investment, which can reflect the health and nutritional status of the mother, as well as broader reproductive strategies in mammals. Calcium‐normalized strontium (Sr) and barium (Ba) concentrations in the growth layers of mammalian teeth differ for nursing animals and those consuming non‐milk foods, thus can be used to estimate age‐at‐weaning. To date, this approach has been used only for terrestrial animals, and almost exclusively for primates.The goal of this study was to determine whether Sr and Ba concentrations in the cementum of Pacific walrus Odobenus rosmarus divergens teeth can be used to estimate weaning age. Teeth from 107 walruses were analysed using laser ablation inductively coupled plasma mass spectrometry, and calcium‐normalized 88Sr and 137Ba concentrations were quantified.For most walruses, both Sr and Ba concentrations exhibited rapid changes in early life. Ba concentrations matched closely with expected patterns in the published literature, rapidly declining from high to low concentrations (typically from ~10 ppm to ~5 ppm). In contrast, Sr exhibited a pattern opposite to that presented in studies of terrestrial mammals, appearing nearly identical to Ba (typically declining from ~400 ppm to ~200 ppm). To explain these findings, we present conceptual models of the factors generating weaning signals in Sr and Ba for terrestrial mammals, as well as a new, hypothetical model for walruses. Both a visual and mathematical approach to weaning age estimation indicated a median weaning age of walruses at the end of the second year of life (in the second dark layer of the tooth cementum), with many walruses estimated to have weaned in their third year of life, and a smaller group weaning in their fourth or fifth year. This is later than expected, given a published estimate of walrus weaning at 18–24 months.These results do not conclusively support the use of tooth Sr and Ba for estimating weaning age in walruses, and further research is warranted to better understand the drivers of the observed patterns of Ba and Sr accumulation in walrus teeth.

Spatial and seasonal patterns of communal latrine use by spotted hyenas (Crocuta crocuta) reflect a seasonal resource defense strategy

Communal marking sites, or latrines, appear to play an important role in intraspecific communication and social dynamics in a wide range of mammal species. The spatial distribution of latrines can provide clues to their function and has been well documented in a number of species. Latrine use may vary considerably through time, however, and a more comprehensive approach to their study that considers spatial and seasonal patterns of use is required to understand more fully the costs and benefits of latrine use, and hence their adaptive significance. This study investigated spatial and seasonal patterns of latrine use by spotted hyena (Crocuta crocuta) in northern Botswana, examining their potential role in resource defense. Latrine characteristics and hyena activity were monitored to test the influence of season and location (relative to clan territories and roads) on latrine use. We conducted monthly scat counts (at 78 latrines) and continuously recorded hyena visitation (to 50 latrines) in five clan home ranges, demonstrating clear seasonal patterns in latrine use. Latrines were smaller in the wet season (November-March), resulting from fewer visits by hyenas, reduced scat accumulation, and the seasonal activity of coprophagous beetles. We speculate that such a seasonal pattern may be driven by reduced competition for food during the wet season. Latrines located within core clan areas were no larger or more frequently used than those in home-range boundary areas, but hyenas did preferentially place latrines alongside roads and were more likely to reuse road-side latrines in subsequent years. This pattern was not due to observer detection bias and adds to the growing body of literature on the impact that roads and other anthropogenic features have on the communication and movement ecology of wild animals. Although most mammals use communal marking sites, very little is known about their function and detailed patterns of use in many species. We investigated latrine use in spotted hyena (Crocuta crocuta) and describe spatial and temporal marking patterns that are consistent with optimizing scent longevity and detection. Spatially, hyenas preferentially located latrines along the edge of man-made vehicle tracks, which may increase signal detection and transmission. Seasonal marking patterns suggest that hyenas optimize their communication by concentrating activity in the dry season, thereby avoiding the disruptive effects of coprophagous dung beetles and rain, and focusing activity during periods when food resources are expected to be scarcer. These results demonstrate seasonal and spatial optimization of communication, including in response to novel anthropogenic features in the environment such as roads, advancing our understanding of communication strategies in mammals more broadly.

GIGYF2 and 4EHP Inhibit Translation Initiation of Defective Messenger RNAs to Assist Ribosome-Associated Quality Control

Ribosome-associated quality control (RQC) pathways protect cells from toxicity caused by incomplete protein products resulting from translation of damaged or problematic mRNAs. Extensive work in yeast has identified highly conserved mechanisms that lead to degradation of faulty mRNA and partially synthesized polypeptides. Here we used CRISPR-Cas9-based screening to search for additional RQC strategies in mammals. We found that failed translation leads to specific inhibition of translation initiation on that message. This negative feedback loop is mediated by two translation inhibitors, GIGYF2 and 4EHP. Model substrates and growth-based assays established that inhibition of additional rounds of translation acts in concert with known RQC pathways to prevent buildup of toxic proteins. Inability to block translation of faulty mRNAs and subsequent accumulation of partially synthesized polypeptides could explain the neurodevelopmental and neuropsychiatric disorders observed in mice and humans with compromised GIGYF2 function.

TGF-β Signaling Promotes Tissue Formation during Cardiac Valve Regeneration in Adult Zebrafish

Cardiac valve disease can lead to severe cardiac dysfunction and is thus a frequent cause of morbidity and mortality. Its main treatment is valve replacement, which is currently greatly limited by the poor recellularization and tissue formation potential of the implanted valves. As we still lack suitable animal models to identify modulators of these processes, here we used adult zebrafish and found that, upon valve decellularization, they initiate a rapid regenerative program that leads to the formation of new functional valves. After injury, endothelial and kidney marrow-derived cells undergo cell cycle re-entry and differentiate into new extracellular matrix-secreting valve cells. The TGF-β signaling pathway promotes the regenerative process by enhancing progenitor cell proliferation as well as valve cell differentiation. These findings reveal a key role for TGF-β signaling in cardiac valve regeneration and establish the zebrafish as a model to identify and test factors promoting cardiac valve recellularization and growth.

Antiviral defense in salmonids – Mission made possible?

Viral diseases represent one of the major threats for salmonid aquaculture. Survival from viral infections are highly dependent on host innate antiviral immune defense, where interferons are of crucial importance. Neutralizing antibodies and T cell effector mechanisms mediate long-term antiviral protection. Despite an immune cell repertoire comparable to higher vertebrates, farmed fish often fail to mount optimal antiviral protection. In the quest to multiply and spread, viruses utilize a variety of strategies to evade or escape the host immune system. Understanding the specific interplay between viruses and host immunity at depth is crucial for developing successful vaccination and treatment strategies in mammals. However, this knowledge base is still limited for pathogenic fish viruses. Here, we have focused on five RNA viruses with major impact on salmonid aquaculture: Salmonid alphavirus, Infectious salmon anemia virus, Infectious pancreatic necrosis virus, Piscine orthoreovirus and Piscine myocarditis virus. This review explore the protective immune responses that salmonids mount to these viruses and the existing knowledge on how the viruses counteract and/or bypass the immune response, including their IFN antagonizing effects and their mechanisms to establish persisting infections.

Hanging out in tents: social structure, group stability, male behavior, and their implications for the mating system of Ectophylla alba (Chiroptera: Phyllostomidae)

Bats show the greatest variety of mating strategies in mammals. Social structure can be influenced by roost characteristics, for example, if the roost is defendable and its availability limited, it becomes an important resource that partially determines the mating system type. In the species that use tents as roosting sites, it has been suggested that males can defend the tent in order to attract and have access to females. Ectophylla alba is an obligate and exclusive tent user, and it has to build tents periodically. Its mating system has been classified as polygyny by its resource defense, and it has a temporary group structure of one male and several females. This study seeks to determine the composition and stability of the groups of this species and to learn whether males defend the tent or the females in it in order to gain copulations. This study was conducted in 2006 in Tirimbina, Biological Reserve in Sarapiqui, Costa Rica, where groups of bats were captured (N = 38). The individuals were marked (N = 98), and their reproductive status was determined. The behavior of the individuals was recorded with video cameras and infrared light (300 h total). Throughout the year, some individuals were more closely associated to other individuals, determining that groups are stable independent of the reproductive season. The proportion of males in the groups does not vary according to reproductive season, and in most groups, there is more than one adult male. The males spend different amounts of time in the tents and do not show antagonistic behavior with other members of the group. Based on the social structure, the classification of the mating system should change to “a stable group of several males and females,” which may be confirmed in the near future by the results of an ongoing paternity study.

How do diet and body mass drive reproductive strategies in mammals?

How do diet and body mass drive reproductive strategies in mammals?

Growth overshoot and seasonal size changes in the skulls of two weasel species.

Ontogenetic changes in mammalian skulls are complex. For a very few species (i.e. some Sorex shrews), these also include seasonally driven, bidirectional size changes within individuals, presumably to reduce energy requirements during low resource availabilities. These patterns are poorly understood, but are likely most pronounced in high-metabolic species with limited means for energy conservation. We used generalized additive models to quantify the effect of location, Julian day, age and sex on the length and depth of 512 and 847 skulls of stoat (Mustela erminea) and weasel (M. nivalis) specimens collected throughout the northern hemisphere. Skull length of both species varies between sexes and geographically, with stoat skull length positively correlated with latitude. Both species demonstrate seasonal and ontogenetic patterns, including a rare, absolute growth overshoot in juvenile braincase depth. Standardized braincase depths of both species peak in their first summer, then decrease in their first winter, followed by a remarkable regrowth that peaks again during their second summer. This seasonal pattern varies in magnitude and timing between geographical regions and the sexes, matching predictions of Dehnel's phenomenon. This suggests implications for the evolution of over-wintering strategies in mammals, justifying further research on their mechanisms and value, with implications for applied osteology research.

Retinoic Acid Signaling Mediates Hair Cell Regeneration by Repressing p27kip and sox2 in Supporting Cells.

Hair cells are the specialized mechanosensory cells of the inner ear that capture auditory and balance sensory input. Hair cells die after acoustic trauma, ototoxic drugs or aging diseases, leading to progressive hearing loss. Mammals, in contrast to zebrafish, lack the ability to regenerate hair cells. Here, we find that retinoic acid (RA) pathway is required for hair cell regeneration in vivo in the zebrafish inner ear and lateral line. RA pathway is activated very early upon hair cell loss, promotes cell proliferation of progenitor cells, and regulates two key genes, p27(kip) and sox2. Our results position RA as an essential signal for hair cell regeneration with relevance in future regenerative strategies in mammals.

Sperm competition drives the evolution of suicidal reproduction in mammals

Suicidal reproduction (semelparity) has evolved in only four genera of mammals. In these insectivorous marsupials, all males die after mating, when failure of the corticosteroid feedback mechanism elevates stress hormone levels during the mating season and causes lethal immune system collapse (die-off). We quantitatively test and resolve the evolutionary causes of this surprising and extreme life history strategy. We show that as marsupial predators in Australia, South America, and Papua New Guinea diversified into higher latitudes, seasonal predictability in abundance of their arthropod prey increased in multiple habitats. More-predictable prey peaks were associated with shorter annual breeding seasons, consistent with the suggestion that females accrue fitness benefits by timing peak energy demands of reproduction to coincide with maximum food abundance. We demonstrate that short mating seasons intensified reproductive competition between males, increasing male energy investment in copulations and reducing male postmating survival. However, predictability of annual prey cycles alone does not explain suicidal reproduction, because unlike insect abundance, peak ovulation dates in semelparous species are often synchronized to the day among years, triggered by a species-specific rate of change of photoperiod. Among species with low postmating male survival, we show that those with suicidal reproduction have shorter mating seasons and larger testes relative to body size. This indicates that lethal effort is adaptive in males because females escalate sperm competition by further shortening and synchronizing the annual mating period and mating promiscuously. We conclude that precopulatory sexual selection by females favored the evolution of suicidal reproduction in mammals.

Lactating mice (Mus musculus) exhibit compensatory flexibility in gut morphology in response to reduced dietary protein

Protein affects key life-history traits, and deficiencies in this nutrient may have selected for the ability to invoke physiological or morphological mechanisms to aid nutrient assimilation. I examined the effect of dietary protein on gut characters in lactating mice (Mus musculus L., 1758) and predicted that mice, to improve assimilation efficiency, would increase the mass of the stomach and small intestine and (or) increase food retention in these organs. Mice were maintained on isocaloric diets differing in protein and carbohydrate content (P:C) during the reproductive period. The hypothesis that food would be preferentially retained was not supported. However, both the stomach and the small intestine responded to low P:C with increased mass, and the small intestine exhibited increased diameter. This study demonstrates that mammalian gut morphology of lactating mice can respond to nutrient availability under conditions of constant energy intake. Further study is needed to determine if gut flexibility in response to decreasing P:C levels results in improved nitrogen assimilation efficiency and if this response is a general strategy of mammals or is limited to those with particular breeding strategies.

Genetic labeling of neuronal subsets through enhancer trapping in mice.

The ability to label, visualize, and manipulate subsets of neurons is critical for elucidating the structure and function of individual cell types in the brain. Enhancer trapping has proved extremely useful for the genetic manipulation of selective cell types in Drosophila. We have developed an enhancer trap strategy in mammals by generating transgenic mice with lentiviral vectors carrying single-copy enhancer-detector probes encoding either the marker gene lacZ or Cre recombinase. This transgenic strategy allowed us to genetically identify a wide variety of neuronal subpopulations in distinct brain regions. Enhancer detection by lentiviral transgenesis could thus provide a complementary method for generating transgenic mouse libraries for the genetic labeling and manipulation of neuronal subsets.

Complex patterns of male alliance formation in a dolphin social network

The formation and maintenance of alliances is regarded as one of the most socially complex male mating strategies in mammals. The prevalence and complexity of these cooperative relationships, however, varies considerably among species as well as within and between populations living in different ecological and social environments. We assessed patterns of alliance formation for Indo-Pacific bottlenose dolphins, Tursiops aduncus, in Port Stephens, New South Wales, Australia, to investigate the stability of these alliances, the structure of associations, as well as variation in schooling patterns among males. Our results showed that association patterns among males within this population showed considerable variability. Males either formed strong and enduring alliances that lasted for at least 8 years with minimal partner switching, or less stable partnerships within a much larger male social network. Male alliances with the strongest levels of association within a given time period were significantly more likely to maintain their relationships over the long term compared with alliances with lower levels of association. Males in stable alliances also associated in significantly smaller schools than males who formed less stable alliance partnerships. Finally, we found that alliances consisting of more related males did not persist longer than alliances between unrelated individuals. Our study suggests that intrapopulation variation in male alliance formation in dolphins likely reflects different mating strategies adopted as individual responses to their complex fission–fusion social environment.

Roles of long, non-coding RNA in chromosome-wide transcription regulation: Lessons from two dosage compensation systems

A large part of higher eukaryotic genomes is transcribed into RNAs lacking any significant open reading frame. This "non-coding part" has been shown to actively contribute to regulating gene expression, but the mechanisms are largely unknown. Particularly instructive examples are provided by the dosage compensation systems, which assure that the single X chromosome in male cells and the two X chromosomes in female cells give rise to similar amounts of gene product. Although this is achieved by very different strategies in mammals and fruit flies, long, non-coding RNAs (lncRNAs) are involved in both cases. Here we summarize recent progress towards unraveling the mechanisms, by which the Xist and roX RNAs mediate the selective association of regulators with individual target chromosomes, to initiate dosage compensation in mammals and fruit flies, respectively.