Traits In Mammals Research Articles

Little impact of new mutations on mammalian trait variation.

New mutations provide the source of all genetic variation but their impact on trait variation remains poorly understood. A new study published in PLOS Biology addresses this question, finding that new mutations exert only weak effects on some traits in mice.

High frequency hearing: A uniquely mammalian trait for sound localization.

High frequency hearing: A uniquely mammalian trait for sound localization.

Epigenetic predictors of species maximum life span and other life-history traits in mammals.

By analyzing 15,000 samples from 348 mammalian species, we derive DNA methylation (DNAm) predictors of maximum life span (R = 0.89), gestation time (R = 0.96), and age at sexual maturity (R = 0.85). Our maximum life-span predictor indicates a potential innate longevity advantage for females over males in 17 mammalian species including humans. The DNAm maximum life-span predictions are not affected by caloric restriction or partial reprogramming. Genetic disruptions in the somatotropic axis such as growth hormone receptors have an impact on DNAm maximum life span only in select tissues. Cancer mortality rates show no correlation with our epigenetic estimates of life-history traits. The DNAm maximum life-span predictor does not detect variation in life span between individuals of the same species, such as between the breeds of dogs. Maximum life span is determined in part by an epigenetic signature that is an intrinsic species property and is distinct from the signatures that relate to individual mortality risk.

Two-stage evolution of mammalian adipose tissue thermogenesis.

Brown adipose tissue (BAT) is a heater organ that expresses thermogenic uncoupling protein 1 (UCP1) to maintain high body temperatures during cold stress. BAT thermogenesis is considered an overarching mammalian trait, but its evolutionary origin is unknown. We show that adipose tissue of marsupials, which diverged from eutherian mammals ~150 million years ago, expresses a nonthermogenic UCP1 variant governed by a partial transcriptomic BAT signature similar to that found in eutherian beige adipose tissue. We found that the reconstructed UCP1 sequence of the common eutherian ancestor displayed typical thermogenic activity, whereas therian ancestor UCP1 is nonthermogenic. Thus, mammalian adipose tissue thermogenesis may have evolved in two distinct stages, with a prethermogenic stage in the common therian ancestor linking UCP1 expression to adipose tissue and thermal stress. We propose that in a second stage, UCP1 acquired its thermogenic function specifically in eutherians, such that the onset of mammalian BAT thermogenesis occurred only after the divergence from marsupials.

Wild Baboons Groom Objects with Fur: Implications for Infant Corpse Carrying in Primates?

Nonhuman primates demonstrate great behavioral diversity in their responses to death, yet the most prevalent of these—infant corpse carrying—remains poorly understood. While mothers are the most frequent carriers, corpse carrying can be performed by non-mothers, and heterospecifics’ corpses are also carried. We propose a new hypothesis to explain, in part, non-maternal corpse carrying, the ‘mammalian cues hypothesis,’ and experimentally test it in a population of wild baboons. The mammalian-cues hypothesis argues that evolutionary pressures on maternal responsiveness have created a generalized attraction towards mammalian-typical traits in mammals of both sexes. This attraction may drive interest in inanimate objects (including corpses) that display mammalian cues. To test this, we presented objects that varied in mammalian traits to wild chacma baboons (Papio ursinus) and recorded their behavioral responses. Contrary to our hypothesis, baboons handled all objects (i.e., with or without mammalian traits) for similar lengths of time. However, in partial support of our hypothesis, baboons groomed the objects with fur—even those without any other mammalian traits—and explored them in a less destructive manner. We caution that infant corpse grooming by non-mothers in primates may be indicative of the visual and tactile stimuli the corpse presents rather than an interest in death or a reflection of social bonds.

The environmental conditions of endemism hotspots shape the functional traits of mammalian assemblages.

Endemic (small-ranged) species are distributed non-randomly across the globe. Regions of high topography and stable climates have higher endemism than flat, climatically unstable regions. However, it is unclear how these environmental conditions interact with and filter mammalian traits. Here, we characterize the functional traits of highly endemic mammalian assemblages in multiple ways, testing the hypothesis that these assemblages are trait-filtered (less functionally diverse) and dominated by species with traits associated with small range sizes. Compiling trait data for more than 5000 mammal species, we calculated assemblage means and multidimensional functional metrics to evaluate the distribution of traits across each assemblage. We then related these metrics to the endemism of global World Wildlife Fund ecoregions using linear models and phylogenetic fourth-corner regression. Highly endemic mammalian assemblages had small average body masses, low fecundity, short lifespans and specialized habitats. These traits relate to the stable climate and rough topography of endemism hotspots and to mammals' ability to expand their ranges, suggesting that the environmental conditions of endemism hotspots allowed their survival. Furthermore, species living in endemism hotspots clustered near the edges of their communities' functional spaces, indicating that abiotic trait filtering and biotic interactions act in tandem to shape these communities.

Detection of 15-bp Indel of HIAT1 Gene and Its Association with Morphometric Traits in Different Goat Populations of Bangladesh

Morphometrics are vital quantitative features for production performance and can affect body size. Hippocampus abundant transcript 1 (HIAT1) gene belongs to the major facilitator superfamily that has specific association with growth related traits in mammals including goat. This study was conducted to investigate possible association between 15-bp insertion/deletion (indel) polymorphism of HIAT1 gene and morphometric traits in different goat populations of Bangladesh. A total of 288 blood samples were collected from Black Bengal goat (BBG), Jamunapari (JP) and Black Bengal cross (BBC) populations. One pair of primer was used to amplify HIAT1 gene fragment that harbored 15-bp indel polymorphism. PCR amplification detected insertion (II), deletion (DD) and heterozygous (ID) genotypes. The II, ID, and DD genotype frequencies were 0.16, 0.44, and 0.40 respectively in BBG populations where the corresponding genotype frequencies were 0.00, 0.47, and 0.53 in JP and 0.11, 0.40, and 0.49 in BBC goat populations. Overall, both the DD and ID genotypes were predominant than II individuals in the studied goat populations. The studied morphometric traits differed significantly among the three goat populations (P<0.01) as well as in different coat color variants of BBG (P<0.05). However, rump width (P<0.001) and rump length (P<0.01) were significantly associated with 15-bp indel genotypes in BBG population and wither height and rump height were significantly (P<0.01) associated in BBC. In conclusion, this study revealed the exitance of 15-bp indel polymorphism in the studied goat populations and its influence on some morphometric traits was found.

Comprehensive analyses of 435 goat transcriptomes provides insight into male reproduction

A systematic analysis of genes related to reproduction is crucial for obtaining a comprehensive understanding of the molecular mechanisms that underlie male reproductive traits in mammals. Here, we utilized 435 goat transcriptome datasets to unveil the testicular tissue-specific genes (TSGs), allele-specific expression (ASE) genes and their uncharacterized transcriptional features related to male goat reproduction. Results showed a total of 1790 TSGs were identified in goat testis, which was the most among all tissues. GO enrichment analyses suggested that testicular TSGs were mainly involved in spermatogenesis, multicellular organism development, spermatid development, and flagellated sperm motility. Subsequently, a total of 95 highly conserved TSGs (HCTSGs), 508 middle conserved TSGs (MCTSGs) and 42 no conserved TSGs (NCTSGs) were identified in goat testis. GO enrichment analyses suggested that the HCTSGs and MCTSGs has a more important association with male reproduction than NCTSGs. Additionally, we identified 644 ASE genes, including 88 tissue-specific ASE (TS-ASE) genes (e.g., FSIP2, TDRD9). GO enrichment analyses indicated that both ASE genes and TS-ASE genes were associated with goat male reproduction. Overall, this study revealed an extensive gene set involved in the regulation of male goat reproduction and their dynamic transcription patterns. Data reported here provide valuable insights for a further improvement of the economic benefits of goats as well as future treatments for male infertility.

Adverse effects of the dietary supplement berberine studied on ants as models

An extract of Berberis plants is nowadays used as a dietary supplement as well as for treating several medical symptoms, e.g., mostly for regulating glycemia, lipid metabolism and central nervous system disorders. Few or no information has so far been reported about side effects of berberine on behavioral and physiological-linked traits. We thus investigated on the potential adverse effects of the alkaloid berberine by using the ant Myrmica sabuleti as a model. We found that berberine decreased the ant’s food intake, activity, locomotion, and sensory perception, but did not impact their social interactions, cognition, learning and memorization. The ants did not adapt themselves to the side effect of berberine on their locomotion. They did not develop strong dependence on berberine consumption. After weaning, the behavioral effect of a diet with berberine linearly decreased until it vanished in 15 – 18 hours. Researches to assess the effect of berberine on various associated behavioral and physiological traits in mammals and in humans are still needed in order to draw a complete safety profile of this substance.

DNA methylation networks underlying mammalian traits.

Using DNA methylation profiles (n = 15,456) from 348 mammalian species, we constructed phyloepigenetic trees that bear marked similarities to traditional phylogenetic ones. Using unsupervised clustering across all samples, we identified 55 distinct cytosine modules, of which 30 are related to traits such as maximum life span, adult weight, age, sex, and human mortality risk. Maximum life span is associated with methylation levels in HOXL subclass homeobox genes and developmental processes and is potentially regulated by pluripotency transcription factors. The methylation state of some modules responds to perturbations such as caloric restriction, ablation of growth hormone receptors, consumption of high-fat diets, and expression of Yamanaka factors. This study reveals an intertwined evolution of the genome and epigenome that mediates the biological characteristics and traits of different mammalian species.

The relationship between OXT gene polymorphisms and reproductive hormones in pregnant and lactating Awassi Ewes.

Numerous genetic loci interact intricately to control reproduction in mammals. The oxytocin gene (OXT) is a promising candidate for reproductive traits in mammals. Previously, sheep and goats have been studied for the presence of the OXT polymorphism. As of yet, no polymorphisms have been identified in the OXT gene of Awassi sheep. Thus, this study was conducted to determine the effects of OXT polymorphism and litter size on reproductive hormones in pregnant and lactating Awassi ewes. This study evaluated 232 ewes aged 3 and 4 years (123 single-progeny ewes and 109 twin-producing ewes). Serum was collected to measure reproductive hormones using ELISA kits manufactured by ELK Biotechnology. DNA was extracted from sheep blood for genotyping and sequencing to identify variations in OXT gene (exon 2, 266bp). Genotyping analysis revealed three genotypes within 266bp: CC, CA, and AA. Sequence analysis revealed a novel mutation in exon 2: 188C > A. Statistical analysis showed significant associations between the 188C > A SNP and phenotypic traits. Twin-pregnant ewes carrying CC genotypes had higher estrogen, progesterone, and follicle-stimulating hormone/luteinizing hormone levels (65.86 ± 3.87) (pg/mL), (6.51 ± 0.39) (ng/mL), and (20.22 ± 1.27) (ng/mL)/( 23.37 ± 2.14) (ng/mL) respectively, compared to CA and AA genotypes in the fourth month of twin-pregnant ewes compared to single-pregnant ewes. This study found that the 188C > A SNP negatively affected reproductive hormone levels in Awassi sheep. These findings provide breeders with a new insight into the sheep OXT gene, useful for future breeding.

Evolutionary constraint and innovation across hundreds of placental mammals.

Zoonomia is the largest comparative genomics resource for mammals produced to date. By aligning genomes for 240 species, we identify bases that, when mutated, are likely to affect fitness and alter disease risk. At least 332 million bases (~10.7%) in the human genome are unusually conserved across species (evolutionarily constrained) relative to neutrally evolving repeats, and 4552 ultraconserved elements are nearly perfectly conserved. Of 101 million significantly constrained single bases, 80% are outside protein-coding exons and half have no functional annotations in the Encyclopedia of DNA Elements (ENCODE) resource. Changes in genes and regulatory elements are associated with exceptional mammalian traits, such as hibernation, that could inform therapeutic development. Earth's vast and imperiled biodiversity offers distinctive power for identifying genetic variants that affect genome function and organismal phenotypes.

Evolution of Longevity as a Species-Specific Trait in Mammals

From the evolutionary point of view, the priority problem for an individual is not longevity, but adaptation to the environment associated with the need for survival, food supply, and reproduction. We see two main vectors in the evolution of mammals. One is a short lifespan and numerous offspring ensuring reproductive success (r-strategy). The other one is development of valuable skills in order compete successfully (K-strategy). Species with the K-strategy should develop and enhance specific systems (anti-aging programs) aimed at increasing the reliability and adaptability, including lifespan. These systems are signaling cascades that provide cell repair and antioxidant defense. Hence, any arbitrarily selected long-living species should be characterized by manifestation to a different extent of the longevity-favoring traits (e.g., body size, brain development, sociality, activity of body repair and antioxidant defense systems, resistance to xenobiotics and tumor formation, presence of neotenic traits). Hereafter, we will call a set of such traits as the gerontological success of a species. Longevity is not equivalent to the evolutionary or reproductive success. This difference between these phenomena reaches its peak in mammals due to the development of endothermy and cephalization associated with the cerebral cortex expansion, which leads to the upregulated production of oxidative radicals by the mitochondria (and, consequently, accelerated aging), increase in the number of non-dividing differentiated cells, accumulation of the age-related damage in these cells, and development of neurodegenerative diseases. The article presents mathematical indicators used to assess the predisposition to longevity in different species (including the standard mortality rate and basal metabolic rate, as well as their derivatives). The properties of the evolution of mammals (including the differences between modern mammals and their ancestral forms) are also discussed.

Vitamin C deficiency reveals developmental differences between neonatal and adult hematopoiesis.

Hematopoiesis, a process that results in the differentiation of all blood lineages, is essential throughout life. The production of 1x1012 blood cells per day, including 200x109 erythrocytes, is highly dependent on nutrient consumption. Notably though, the relative requirements for micronutrients during the perinatal period, a critical developmental window for immune cell and erythrocyte differentiation, have not been extensively studied. More specifically, the impact of the vitamin C/ascorbate micronutrient on perinatal as compared to adult hematopoiesis has been difficult to assess in animal models. Even though humans cannot synthesize ascorbate, due to a pseudogenization of the L-gulono-γ-lactone oxidase (GULO) gene, its generation from glucose is an ancestral mammalian trait. Taking advantage of a Gulo-/- mouse model, we show that ascorbic acid deficiency profoundly impacts perinatal hematopoiesis, resulting in a hypocellular bone marrow (BM) with a significant reduction in hematopoietic stem cells, multipotent progenitors, and hematopoietic progenitors. Furthermore, myeloid progenitors exhibited differential sensitivity to vitamin C levels; common myeloid progenitors and megakaryocyte-erythrocyte progenitors were markedly reduced in Gulo-/- pups following vitamin C depletion in the dams, whereas granulocyte-myeloid progenitors were spared, and their frequency was even augmented. Notably, hematopoietic cell subsets were rescued by vitamin C repletion. Consistent with these data, peripheral myeloid cells were maintained in ascorbate-deficient Gulo-/- pups while other lineage-committed hematopoietic cells were decreased. A reduction in B cell numbers was associated with a significantly reduced humoral immune response in ascorbate-depleted Gulo-/- pups but not adult mice. Erythropoiesis was particularly sensitive to vitamin C deprivation during both the perinatal and adult periods, with ascorbate-deficient Gulo-/- pups as well as adult mice exhibiting compensatory splenic differentiation. Furthermore, in the pathological context of hemolytic anemia, vitamin C-deficient adult Gulo-/- mice were not able to sufficiently increase their erythropoietic activity, resulting in a sustained anemia. Thus, vitamin C plays a pivotal role in the maintenance and differentiation of hematopoietic progenitors during the neonatal period and is required throughout life to sustain erythroid differentiation under stress conditions.

Comparative transcriptome analysis reveals molecular adaptations underlying distinct immunity and inverted resting posture in bats.

Understanding how natural selection shapes unique traits in mammals is a central topic in evolutionary biology. The mammalian order Chiroptera (bats) is attractive for biologists as well as the general public due to their specific traits of extraordinary immunity and inverted resting posture. However, genomic resources for bats that occupy key phylogenetic positions are not sufficient, which hinders comprehensive investigation of the molecular mechanisms underpinning the origin of specific traits in bats. Here, we sequenced the transcriptomes of 5 bats that are phylogenetically divergent and occupy key positions in the phylogenetic tree of bats. In combination with the available genomes of 19 bats and 21 other mammals, we built a database consisting of 10918 one-to-one ortholog genes and reconstructed phylogenetic relationships of these mammals. We found that genes related to immunity, bone remodeling, and cardiovascular system are targets of natural selection along the ancestral branch of bats. Further analyses revealed that the T cell receptor signaling pathway involved in immune adaptation is specifically enriched in bats. Moreover, molecular adaptations of bone remodeling, cardiovascular system, and balance sensing may help to explain the reverted resting posture in bats. Our study provides valuable transcriptome resources, enabling us to tentatively identify genetic changes associated with bat-specific traits. This work is among the first to advance our understanding of the molecular underpinnings of inverted resting posture in bats, which could provide insight into healthcare applications such as hypertension in humans.

Evaluating the potential of improving sperm quality traits in farmed Arctic charr (Salvelinus alpinus) using selective breeding

Arctic charr (Salvelinus alpinus) is a high-value species for the Nordic aquaculture. The highly variable reproductive performance that is commonly observed in commercial farms is hindering the expansion of the Arctic charr industry in Sweden. Traits related to sperm motility (total motility; curvilinear velocity; average path velocity; straight-line velocity) and concentration can play a pivotal role in male fertility. Selective breeding practices could offer solutions and contribute to improving male fertility. The current study aimed to investigate the magnitude of genetic variance for sperm quality traits in a selectively bred population of Arctic charr from Sweden and evaluate the possibility of their improvement through selection. Sperm motility and concentration were recorded using a computer-assisted semen analysis (CASA) system and a NucleoCounter, respectively, in over 400 males from year-class 2017. Double digest restriction-site associated DNA sequencing (ddRAD-seq) was applied in a subset of the recorded animals (n = 329), resulting in the detection of over 5000 single nucleotide polymorphisms (SNPs). Moderate heritability estimates were obtained for the recorded semen traits using both pedigree (0.21–0.32; SE 0.09) and genomic (0.23–0.26; SE 0.09) relationship matrices. A genome-wide association study (GWAS) detected a single SNP significantly associated (P < 1e-05) with total sperm motility on chromosome LG7 in relatively close proximity (500 Kb) to PTPN11 a gene previously associated with sperm quality traits in mammals. Moreover, weighted single-step genomic best linear unbiased prediction (WssGBLUP) pinpointed genomic regions explaining more than 3 % of the additive genetic variance for both the motility traits and the sperm concentration. Finally, the efficiency of genomic prediction was tested using a 3-fold cross-validation scheme. Higher prediction accuracy for total motility and velocities (both curvilinear and average path) was obtained using genomic information (0.26–0.29, SE 0.03–0.06) compared to pedigree (0.20–0.28, SE 0.04–0.07), while for sperm concentration a pedigree-based model (0.22 SE 0.03) was more efficient than the genomic model (0.14 SE 0.04). Overall, our results indicate that the recorded sperm quality traits are heritable, and could be improved through selective breeding practices.

Conserved and Taxon-Specific Patterns of Phenotypic Modularity in the Mammalian Dentition.

SynopsisPrevious genotype:phenotype mapping of the mouse and primate dentition revealed the presence of pre- and post-canine modules in mice and anthropoid primates, as well as molar and premolar submodules in anthropoid primates. We estimated phenotypic correlation matrices for species that sample broadly across Mammalia to test the hypothesis that these modules exist across a broader range of taxa and thereby represent a conserved mammalian trait. We calculated phenotypic correlation matrices from linear dental measurements of 419 individual specimens representing 5 species from 4 mammalian orders: Artiodactyla (Odocoileus hemionus), Carnivora (Canis latrans and Ursus americanus), Didelphimorphia (Didelphis virginiana), and Primates (Colobus guereza). Our results based on hierarchical clustering indicate a generally higher correlation within incisors and among post-canine teeth. However, the post-canine phenotypic correlation matrices do not consistently exhibit the premolar and molar submodularity observed in anthropoid primates. Additionally, we find evidence of sex differences in the Odocoileus phenotypic correlation matrices: Males of this species exhibit overall higher inter-trait correlations compared to females. Our overall findings support the interpretation that incisors and post-canine dentition represent different phenotypic modules, and that this architecture may be a conserved trait for mammals.

A remarkable rodent: Regeneration and reproduction in spiny mice (Acomys).

Although certain organisms are chosen and employed to better understand a specific problem in biology (so-called model organisms), sometimes an animal model reveals its' biomedical importance by happenstance. In many ways, the advent of spiny mice (Acomys) as an emerging model to study regeneration and menstruation stands as a case study in scientific pseudoserendipity (Diaz de Chumaceiro, 1995). As we recount in this chapter, the discovery of these phenotypes, while not entirely accidental, was nonetheless unexpected. In addition to recounting how we uncovered these unusual mammalian traits, we outline recent work by our groups and others that has begun to outline the cellular and genetic mechanisms underlying bonafide mammalian tissue regeneration and a human-like mode of reproduction in spiny mice.

Phenotyping in the era of genomics: MaTrics\u2014a digital character matrix to document mammalian phenotypic traits

A new and uniquely structured matrix of mammalian phenotypes, MaTrics (Mammalian Traits for Comparative Genomics) in a digital form is presented. By focussing on mammalian species for which genome assemblies are available, MaTrics provides an interface between mammalogy and comparative genomics.MaTrics was developed within a project aimed to find genetic causes of phenotypic traits of mammals using Forward Genomics. This approach requires genomes and comprehensive and recorded information on homologous phenotypes that are coded as discrete categories in a matrix. MaTrics is an evolving online resource providing information on phenotypic traits in numeric code; traits are coded either as absent/present or with several states as multistate. The state record for each species is linked to at least one reference (e.g., literature, photographs, histological sections, CT scans, or museum specimens) and so MaTrics contributes to digitalization of museum collections. Currently, MaTrics covers 147 mammalian species and includes 231 characters related to structure, morphology, physiology, ecology, and ethology and available in a machine actionable NEXUS-format*. Filling MaTrics revealed substantial knowledge gaps, highlighting the need for phenotyping efforts. Studies based on selected data from MaTrics and using Forward Genomics identified associations between genes and certain phenotypes ranging from lifestyles (e.g., aquatic) to dietary specializations (e.g., herbivory, carnivory). These findings motivate the expansion of phenotyping in MaTrics by filling research gaps and by adding taxa and traits. Only databases like MaTrics will provide machine actionable information on phenotypic traits, an important limitation to genomics. MaTrics is available within the data repository Morph·D·Base (www.morphdbase.de).

Increased Reliance on Carbohydrates for Aerobic Exercise in Highland Andean Leaf-Eared Mice, but Not in Highland Lima Leaf-Eared Mice

Exercise is an important performance trait in mammals and variation in aerobic capacity and/or substrate allocation during submaximal exercise may be important for survival at high altitude. Comparisons between lowland and highland populations is a fruitful approach to understanding the mechanisms for altitude differences in exercise performance. However, it has only been applied in very few highland species. The leaf-eared mice (LEM, genus Phyllotis) of South America are a promising taxon to uncover the pervasiveness of hypoxia tolerance mechanisms. Here we use lowland and highland populations of Andean and Lima LEM (P. andium and P. limatus), acclimated to common laboratory conditions, to determine exercise-induced maximal oxygen consumption (O2max), and submaximal exercise metabolism. Lowland and highland populations of both species showed no difference in O2max running in either normoxia or hypoxia. When run at 75% of O2max, highland Andean LEM had a greater reliance on carbohydrate oxidation to power exercise. In contrast, highland Lima LEM showed no difference in exercise fuel use compared to their lowland counterparts. The higher carbohydrate oxidation seen in highland Andean LEM was not explained by maximal activities of glycolytic enzymes in the gastrocnemius muscle, which were equivalent to lowlanders. This result is consistent with data on highland deer mouse populations and suggests changes in metabolic regulation may explain altitude differences in exercise performance.