Rhodopsin Molecular Evolution in Mammals Inhabiting Low Light Environments

The ecological radiation of mammals to inhabit a variety of light environments is largely attributed to adaptive changes in their visual systems. Visual capabilities are conferred by anatomical features of the eyes as well as the combination and properties of their constituent light sensitive pigments. To test whether evolutionary switches to different niches characterized by dim-light conditions coincided with molecular adaptation of the rod pigment rhodopsin, we sequenced the rhodopsin gene in twenty-two mammals including several bats and subterranean mole-rats. We compared these to thirty-seven published mammal rhodopsin sequences, from species with divergent visual ecologies, including nocturnal, diurnal and aquatic groups. All taxa possessed an intact functional rhodopsin; however, phylogenetic tree reconstruction recovered a gene tree in which rodents were not monophyletic, and also in which echolocating bats formed a monophyletic group. These conflicts with the species tree appear to stem from accelerated evolution in these groups, both of which inhabit low light environments. Selection tests confirmed divergent selection pressures in the clades of subterranean rodents and bats, as well as in marine mammals that live in turbid conditions. We also found evidence of divergent selection pressures among groups of bats with different sensory modalities based on vision and echolocation. Sliding window analyses suggest most changes occur in transmembrane domains, particularly obvious within the pinnipeds; however, we found no obvious pattern between photopic niche and predicted spectral sensitivity based on known critical amino acids. This study indicates that the independent evolution of rhodopsin vision in ecologically specialised groups of mammals has involved molecular evolution at the sequence level, though such changes might not mediate spectral sensitivity directly

Molecular evolution of the hyaluronan synthase 2 gene in mammals: implications for adaptations to the subterranean niche and cancer resistance

The naked mole-rat (NMR) Heterocephalus glaber is a unique and fascinating mammal exhibiting many unusual adaptations to a subterranean lifestyle. The recent discovery of their resistance to cancer and exceptional longevity has opened up new and important avenues of research. Part of this resistance to cancer has been attributed to the fact that NMRs produce a modified form of hyaluronan—a key constituent of the extracellular matrix—that is thought to confer increased elasticity of the skin as an adaptation for living in narrow tunnels. This so-called high molecular mass hyaluronan (HMM-HA) stems from two apparently unique substitutions in the hyaluronan synthase 2 enzyme (HAS2). To test whether other subterranean mammals with similar selection pressures also show molecular adaptation in their HAS2 gene, we sequenced the HAS2 gene for 11 subterranean mammals and closely related species, and combined these with data from 57 other mammals. Comparative screening revealed that one of the two putatively important HAS2 substitutions in the NMR predicted to have a significant effect on hyaluronan synthase function was uniquely shared by all African mole-rats. Interestingly, we also identified multiple other amino acid substitutions in key domains of the HAS2 molecule, although the biological consequences of these for hyaluronan synthesis remain to be determined. Despite these results, we found evidence of strong purifying selection acting on the HAS2 gene across all mammals, and the NMR remains unique in its particular HAS2 sequence. Our results indicate that more work is needed to determine whether the apparent cancer resistance seen in NMR is shared by other members of the African mole-rat clade.National Research Foundation (South Africa

Field evidence for colony size and aseasonality of breeding and in Ansell’s mole-rat, Fukomys anselli (Rodentia: Bathyergidae)

Ansell’s mole-rat, Fukomys anselli, is a cooperatively breeding bathyergid endemic to the Lusaka Province of Zambia. During a 12-month field study involving the capture of 33 colonies of mole-rats, the number of occupants, breeding females and sex ratio within colonies were recorded. While thirty of these social groups contained a single breeding queen, three were found to exhibit plural breeding among females, having two queens present simultaneously. Mean±S.E.M. colony size was 8.7±2.2 (range 6–16,n=33). The occurrence of plural breeding and small group size is consistent with the predictions of the aridity food distribution hypothesis for social species inhabiting mesic habitats. The sex ratio of the population was skewed towards females at 1.2:1. The mean mass of adult males was 63.0 ± 18.3 g (range 36.7–110.3, n=87) while that for adult females was 52.9±11.8 g (range 35.1–77.8, n=86). Pregnant and lactating females were found throughout the study period from February 2009 to February 2010, indicating an aseasonal pattern of breeding in this species. Autopsy of individuals (n = 288) from the 33 colonies revealed a total of 19 pregnant females. Nine of these were in the latter stages of pregnancy and mean litter size was determined as 2.7 pups (range 1–4). Collectively, these new data reveal that Fukomys anselli share many similarities in life history and reproductive traits with the phylogentically closely related giant Zambian mole-rat, Fukomys mechowii.A Department of Science and Technology and National Research Foundation SARChI Chair in Mammal Behavioural Ecology and Physiology to NCB. AMS was the recipient of a postdoctoral fellowship from the SARChI chair.http://www.bioone.org/loi/afzoab201

Patterns of Genetic Diversity and Gene Flow Associated With an Aridity Gradient in Populations of Common Mole-rats, Cryptomys hottentotus hottentotus

Genetic adaptation is the change of a population toward a phenotype that best fits the present ecological conditions of the environment it inhabits. As environmental conditions change, allele frequencies shift, resulting in different populations of the same species possessing genetic variation and divergent phenotypes. Cooperatively breeding common mole-rats (Cryptomys hottentotus hottentotus) inhabit environments along an aridity gradient in South Africa, which provides an opportunity for local genetic adaptations to occur. Using one mitochondrial gene (cytochrome b) and 3,540 SNP loci across the whole genome, we determined the phylogenetic relationship, population structure and genetic diversity of five populations of C. h. hottentotus located along an aridity gradient. Mitochondrial data identified population-specific clades that were less distinct in the two mesic populations, potentially indicating historical or recent gene flow, or the retention of ancestral haplotypes. Arid and semi-arid populations formed a distinct cluster from the non-arid populations. Genetic diversity and gene flow were higher in arid-dwelling individuals, suggesting greater connectivity and interactions between colonies in arid regions in comparison to mesic ones. Using an Aridity Index, we determined that isolation by environment, rather than isolation by geographical distance, best explains the genetic distance between the populations. Further analyses using target loci may determine if there are differing underlying genetic adaptations among populations of C. h. hottentotus. These analyses could help unravel population differences in response to environmental factors within a subspecies of bathyergid mole-rat and determine the adaptive capacity of this small nonmigratory subterranean rodent species in response to aridification in the face of climate change

Digging for answers : contributions of density- and frequency-dependent factors on ectoparasite burden in a social mammal

Due to the density-dependent nature of parasite transmission parasites are generally assumed to constrain the evolution of sociality. However, evidence for a correlation between group size and parasite burden is equivocal, particularly for mammals. Host contact rates may be modified by mobility of the host and parasite as well as social barriers. In the current study, we used the common mole-rat (Cryptomys hottentotus hottentotus), a social subterranean rodent, as a model system to investigate the effect of host density and frequency of contact rates on ectoparasite burdens. To address these factors we used a study species that naturally varies in population densities and intergroup contact rates across its geographic range. We found that ectoparasite prevalence, abundance and species richness decreased with increasing host density at a regional scale. At the same time, measures of parasite burden increased with intergroup contact rates. Ectoparasite burdens decreased with colony size at the group level possibly as a result of increased grooming rates. Equating group size with population density might be too simplistic an approach when assessing parasite distributions in social mammals. Our data suggest that frequency-dependent mechanisms may play a much greater role at a population level than density-dependent mechanisms in determining parasite distributions in social species. We suggest that future studies should explicitly consider behavioural mechanisms that may affect parasite distribution.NRF-SAR Chair for Mammalian Behavioural Ecology and Physiology to NCB.University of Pretoria Research Fellowship.http://link.springer.com/journal/4422017-02-26hb201

Reproduction in the East African root rat (Tachyoryctes splendens ; Rodentia : Spalacidae) from Tanzania : the importance of rainfall

The East African root rat, Tachyoryctes splendens (Rüppell, 1835) is a solitary subterranean rodent mole. The present study investigated breeding patterns in both sexes of T. splendens from data collected at monthly intervals over an entire calendar year. The study focused on the analyses from post mortem examination of males and females to assess the presence of foetuses, gonadal histology, reproductive tract morphometrics, measurement of gonadal steroids (plasma progesterone and oestradiol-17β in females and testosterone in males) and field observations (i.e., the presence of infants, juveniles, sub-adults and lactating females). The objective of this study was to assess if the reproductive biology of the root rat reflected the bimodal pattern of rainfall that is characteristic of East Africa. Rainfall has been suggested to trigger breeding in many subterranean rodents and as a consequence, this study aimed to assess the relationship between rainfall and reproductive characteristics of T. splendens. Peaks in mean gonadal mass, increases in concentration of reproductive hormones and the presence of Graafian follicles and corpora lutea in the ovaries of females, and testes mass, seminiferous tubule diameter and testosterone titre mirrored the annual peaks of precipitation at the study area. Together with field observations of the temporal occurrence of pregnancies, infants, juveniles and sub-adults, the data show that T. spendens cues its breeding with the patterns of rainfall, such that offspring are born in the latter half of each rainy season, from April to July and November to December.University of Dar es Salaam [UDSM–World Bank Fund (C1B1) ], Tanzania.South African Department of Science and Technology (DST)/National Research Foundation (NRF) SARChI Chair for Mammal Behavioural Ecology and Physiology, University of Pretoria.http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1469-7998hb201

Hypofunctional TrkA Accounts for the Absence of Pain Sensitization in the African Naked Mole-Rat.

The naked mole-rat is a subterranean rodent lacking several pain behaviors found in humans, rats, and mice. For example, nerve growth factor (NGF), an important mediator of pain sensitization, fails to produce thermal hyperalgesia in naked mole-rats. The sensitization of capsaicin-sensitive TRPV1 ion channels is necessary for NGF-induced hyperalgesia, but naked mole-rats have fully functional TRPV1 channels. We show that exposing isolated naked mole-rat nociceptors to NGF does not sensitize TRPV1. However, the naked mole-rat NGF receptor TrkA displays a reduced ability to engage signal transduction pathways that sensitize TRPV1. Between one- and three-amino-acid substitutions in the kinase domain of the naked mole-rat TrkA are sufficient to render the receptor hypofunctional, and this is associated with the absence of heat hyperalgesia. Our data suggest that evolution has selected for a TrkA variant that abolishes a robust nociceptive behavior in this species but is still compatible with species fitness.This work was supported by a European Research Council grant (grant 294678 Extremeophile Mammal) to G.R.L. E.S.J.S. acknowledges support from the Alexander von Humboldt foundation.This is the final version of the article. It first appeared from Elsevier (Cell Press) via https://doi.org/10.1016/j.celrep.2016.09.03

Molecular evolution of the hyaluronan synthase 2 gene in mammals : implications for adaptations to the subterranean niche and cancer resistance

The naked mole-rat (NMR) Heterocephalus glaber is a unique and fascinating mammal exhibiting many unusual adaptations to a subterranean lifestyle. The recent discovery of their resistance to cancer and exceptional longevity has opened up new and important avenues of research. Part of this resistance to cancer has been attributed to the fact that NMRs produce a modified form of hyaluronan—a key constituent of the extracellular matrix—that is thought to confer increased elasticity of the skin as an adaptation for living in narrow tunnels. This so-called high molecular mass hyaluronan (HMM-HA) stems from two apparently unique substitutions in the hyaluronan synthase 2 enzyme (HAS2). To test whether other subterranean mammals with similar selection pressures also show molecular adaptation in their HAS2 gene, we sequenced the HAS2 gene for 11 subterranean mammals and closely related species, and combined these with data from 57 other mammals. Comparative screening revealed that one of the two putatively important HAS2 substitutions in the NMR predicted to have a significant effect on hyaluronan synthase function was uniquely shared by all African mole-rats. Interestingly, we also identified multiple other amino acid substitutions in key domains of the HAS2 molecule, although the biological consequences of these for hyaluronan synthesis remain to be determined. Despite these results, we found evidence of strong purifying selection acting on the HAS2 gene across all mammals, and the NMR remains unique in its particular HAS2 sequence. Our results indicate that more work is needed to determine whether the apparent cancer resistance seen in NMR is shared by other members of the African molerat clade.DST-NRF SARChI Chair for Behavioural Ecology and Physiology.European Research Council.http://rsbl.royalsocietypublishing2016-05-31hb201

Family wide molecular adaptations to underground life in African mole-rats revealed by phylogenomic analysis

During their evolutionary radiation, mammals have colonized diverse habitats. Arguably the subterranean niche is the most inhospitable of these, characterized by reduced oxygen, elevated carbon dioxide, absence of light, scarcity of food, and a substrate that is energetically costly to burrow through. Of all lineages to have transitioned to a subterranean niche, African mole-rats are one of the most successful. Much of their ecological success can be attributed to a diet of plant storage organs, which has allowed them to colonize climatically varied habitats across sub-Saharan Africa, and has probably contributed to the evolution of their diverse social systems. Yet despite their many remarkable phenotypic specializations, little is known about molecular adaptations underlying these traits. To address this, we sequenced the transcriptomes of seven mole-rat taxa, including three solitary species, and combined new sequences with existing genomic data sets. Alignments of more than 13,000 protein-coding genes encompassed, for the first time, all six genera and the full spectrum of ecological and social variation in the clade. We detected positive selection within the mole-rat clade and along ancestral branches in approximately 700 genes including loci associated with tumorigenesis, aging, morphological development, and sociality. By combining these results with gene ontology annotation and protein–protein networks, we identified several clusters of functionally related genes. This family wide analysis of molecular evolution in mole-rats has identified a suite of positively selected genes, deepening our understanding of the extreme phenotypic traits exhibited by this group.The European Research Council (ERC Starting grant 310482 [EVOGENO]) awarded to S.J.R.; the DST-NRF SARChI Chair of Mammalian Behavioral Ecology and Physiology (grant number 64756) (funds to N.C.B.).http://mbe.oxfordjournals.orghb201

Ten strategies for avoiding and overcoming authorship conflicts in academic publishing

For better or for worse, authorship is a currency in scholarly research and advancement. In scholarly writing, authorship is widely acknowledged as a means of conferring credit but is also tied to concepts such as responsibility and accountability. Authorship is one of the most divisive topics both at the level of the research team and more broadly in the academy and beyond. At present, authorship is often the primary way to assert and receive credit in many scholarly pursuits and domains. Debates rage, publicly but mostly privately, regarding authorship. Here we attempt to clarify key concepts related to authorship informed by our collective experiences and anchored in relevant contemporary literature. Rather than dwelling on the problems, we focus on proactive strategies for creating more just, equitable, and transparent avenues for minimizing conflict around authorship and where there is adequate recognition of the entire process of knowledge generation, synthesis, sharing, and application with partners within and beyond the academy. We frame our ideas around 10 strategies that collectively constitute a roadmap for avoiding and overcoming challenges associated with authorship decisions