Mammalian maxilloturbinal evolution does not reflect thermal biology

The evolution of endothermy in vertebrates is a major research topic in recent decades that has been tackled by a myriad of research disciplines including paleontology, anatomy, physiology, evolutionary and developmental biology. The ability of most mammals to maintain a relatively constant and high body temperature is considered a key adaptation, enabling them to successfully colonize new habitats and harsh environments. It has been proposed that in mammals the anterior nasal cavity, which houses the maxilloturbinal, plays a pivotal role in body temperature maintenance, via a bony system supporting an epithelium involved in heat and moisture conservation. The presence and the relative size of the maxilloturbinal has been proposed to reflect the endothermic conditions and basal metabolic rate in extinct vertebrates. We show that there is no evidence to relate the origin of endothermy and the development of some turbinal bones by using a comprehensive dataset of µCT-derived maxilloturbinals spanning most mammalian orders. Indeed, we demonstrate that neither corrected basal metabolic rate nor body temperature significantly correlate with the relative surface area of the maxilloturbinal. Instead, we identify important variations in the relative surface area, morpho-anatomy, and complexity of the maxilloturbinal across the mammalian phylogeny and species ecology

Social Structure Predicts Genital Morphology in African Mole-Rats

BACKGROUND:African mole-rats (Bathyergidae, Rodentia) exhibit a wide range of social structures, from solitary to eusocial. We previously found a lack of sex differences in the external genitalia and morphology of the perineal muscles associated with the phallus in the eusocial naked mole-rat. This was quite surprising, as the external genitalia and perineal muscles are sexually dimorphic in all other mammals examined. We hypothesized that the lack of sex differences in naked mole-rats might be related to their unusual social structure. METHODOLOGY/PRINCIPAL FINDINGS:We compared the genitalia and perineal muscles in three African mole-rat species: the naked mole-rat, the solitary silvery mole-rat, and the Damaraland mole-rat, a species considered to be eusocial, but with less reproductive skew than naked mole-rats. Our findings support a relationship between social structure, mating system, and sexual differentiation. Naked mole-rats lack sex differences in genitalia and perineal morphology, silvery mole-rats exhibit sex differences, and Damaraland mole-rats are intermediate. CONCLUSIONS/SIGNIFICANCE:The lack of sex differences in naked mole-rats is not an attribute of all African mole-rats, but appears to have evolved in relation to their unusual social structure and reproductive biology

Light Perception in Two Strictly Subterranean Rodents: Life in the Dark or Blue?

BACKGROUND: The African mole-rats (Bathyergidae, Rodentia) are strictly subterranean, congenitally microphthalmic rodents that are hardly ever exposed to environmental light. Because of the lack of an overt behavioural reaction to light, they have long been considered to be blind. However, recent anatomical studies have suggested retention of basic visual capabilities. In this study, we employed behavioural tests to find out if two mole-rat species are able to discriminate between light and dark, if they are able to discriminate colours and, finally, if the presence of light in burrows provokes plugging behaviour, which is assumed to have a primarily anti-predatory function. METHODOLOGY/PRINCIPAL FINDING: We used a binary choice test to show that the silvery mole-rat Heliophobius argenteocinereus and the giant mole-rat Fukomys mechowii exhibit a clear photoavoidance response to full-spectrum ("white"), blue and green-yellow light, but no significant reaction to ultraviolet or red light during nest building. The mole-rats thus retain dark/light discrimination capabilities and a capacity to perceive short to medium-wavelength light in the photopic range of intensities. These findings further suggest that the mole-rat S opsin has its absorption maximum in the violet/blue part of the spectrum. The assay did not yield conclusive evidence regarding colour discrimination. To test the putative role of vision in bathyergid anti-predatory behaviour, we examined the reaction of mole-rats to the incidence of light in an artificial burrow system. The presence of light in the burrow effectively induced plugging of the illuminated tunnel. CONCLUSION/SIGNIFICANCE: Our findings suggest that the photopic vision is conserved and that low acuity residual vision plays an important role in predator avoidance and tunnel maintenance in the African mole-rats

Extended Longevity of Reproductives Appears to be Common in Fukomys Mole-Rats (Rodentia, Bathyergidae)

African mole-rats (Bathyergidae, Rodentia) contain several social, cooperatively breeding species with low extrinsic mortality and unusually high longevity. All social bathyergids live in multigenerational families where reproduction is skewed towards a few breeding individuals. Most of their offspring remain as reproductively inactive “helpers” in their natal families, often for several years. This “reproductive subdivision” of mole-rat societies might be of interest for ageing research, as in at least one social bathyergid (Ansell's mole-rats Fukomys anselli), breeders have been shown to age significantly slower than non-breeders. These animals thus provide excellent conditions for studying the epigenetics of senescence by comparing divergent longevities within the same genotypes without the inescapable short-comings of inter-species comparisons. It has been claimed that many if not all social mole-rat species may have evolved similar ageing patterns, too. However, this remains unclear on account of the scarcity of reliable datasets on the subject. We therefore analyzed a 20-year breeding record of Giant mole-rats Fukomys mechowii, another social bathyergid species. We found that breeders indeed lived significantly longer than helpers (ca. 1.5–2.2fold depending on the sex), irrespective of social rank or other potentially confounding factors. Considering the phylogenetic positions of F. mechowii and F. anselli and unpublished data on a third Fukomys-species (F. damarensis) showing essentially the same pattern, it seems probable that the reversal of the classic trade-off between somatic maintenance and sexual reproduction is characteristic of the whole genus and hence of the vast majority of social mole-rats

Dental peculiarities in the silvery mole-rat: an original model for studying the evolutionary and biological origins of continuous dental generation in mammals

Unravelling the evolutionary and developmental mechanisms that have impacted the mammalian dentition, since more than 200 Ma, is an intricate issue. Interestingly, a few mammal species, including the silvery mole-rat Heliophobius argenteocinereus, are able to replace their dentition by the addition of supernumerary molars at the back of jaw migrating then toward the front. The aim here was to demonstrate the potential interest of further studying this rodent in order to better understand the origins of continuous dental replacement in mammals, which could also provide interesting data concerning the evolution of limited dental generation occurring in first mammals. In the present study, we described the main stages of the dental eruptive sequence in the silvery mole-rat and the associated characteristics of horizontal replacement using X-ray microtomography. This was coupled to the investigation of other African mole-rats which have no dental replacement. This method permitted to establish evidence that the initial development of the dentition in Heliophobius is comparable to what it is observed in most of African mole-rats. This rodent first has premolars, but then identical additional molars, a mechanism convergent to manatees and the pygmy rock-wallaby. Evidence of continuous replacement and strong dental dynamics were also illustrated in Heliophobius, and stressed the need to deeply investigate these aspects for evolutionary, functional and developmental purposes. We also noticed that two groups of extinct non-mammalian synapsids convergently acquired this dental mechanism, but in a way differing from extant mammals. The discussion on the diverse evolutionary origins of horizontal dental replacement put emphasis on the necessity of focusing on biological parameters potentially involved in both continuous and limited developments of teeth in mammals. In that context, the silvery mole-rat could appear as the most appropriate candidate to do so

Life in Burrows Channelled the Morphological Evolution of the Skull in Rodents: the Case of African Mole-Rats (Bathyergidae, Rodentia)

International audienceAfrican mole-rats are fossorial rodents that consist of five chisel-tooth digging genera (Heterocephalus, Heliophobius, Georychus, Fukomys, and Cryptomys) and one scratch digger (Bathyergus). They are characterized by striking physiological, morphological, and behavioral adaptations intimately related to their subterranean life. The influence of their mode of life in shaping the cranial morphology has yet to be evaluated in comparison to other Ctenohystrica, especially fossorial genera, which include the subterranean genera Spalacopus and Ctenomys. In our study, we seek to determine to what extent subterranean life affects the morpho-functional properties of the skull among fossorial ctenohystricans. 3D geometric morphometric analyses were performed on 277 skulls, encompassing 63 genera of Ctenohystrica, and complemented by biomechanical studies. African mole-rats and other subterranean Ctenohystrica, especially chisel-tooth diggers, have a short snout, a wide cranium with enlarged zygomatic arches, and a strongly hystricognathous mandible. Even if convergences are also manifest between most fossorial Ctenohystrica, subterranean rodents departed from the main ctenohystrican allometric trends in having a skull shape less size-dependent, but under stronger directional selection with intense digging activity as a major constraint. African mole-rats, notably chisel-tooth diggers, show important mechanical advantage for the temporalis muscles favoring higher forces at the bite point, while mechanical advantage of the superficial masseter muscles is lower compared to other Ctenohystrica. If subterranean species can be clearly discriminated based on their skull morphology, the intrinsic mosaic of anatomical characters of each genus (e.g., skull, teeth, and muscles) can be understood only in the light of their ecology and evolutionary history

Data from: Parentage analysis of Ansell's mole-rat family groups indicates a high reproductive skew despite relatively relaxed ecological constraints on dispersal

To better understand evolutionary pathways leading to eusociality, interspecific comparisons are needed, which would use a common axis, such as that of reproductive skew, to array species. African mole-rats (Bathyergidae, Rodentia) provide an outstanding model of social evolution because of a wide range of social organizations within a single family; however, their reproductive skew is difficult to estimate, due to their cryptic lifestyle. A maximum skew could theoretically be reached in groups where reproduction is monopolized by a stable breeding pair, but the value could be decreased by breeding-male and breeding-female turnover, shared reproduction and extra-group mating. The frequency of such events should be higher in species or populations inhabiting mesic environments with relaxed ecological constraints on dispersal. To test this prediction, we studied patterns of parentage and relatedness within 16 groups of Ansell's mole-rat (Fukomys anselli) in mesic miombo woodland. Contrary to expectation, there was no shared reproduction (more than one breeder of a particular sex) within the studied groups, and proportion of immigrants and offspring not assigned to current breeding males was low. The within-group parentage and relatedness patterns observed resemble arid populations of ‘eusocial’ Fukomys damarensis, rather than a mesic population of ‘social’ Cryptomys hottentotus. As a possible explanation, we propose that the extent ecological conditions affect reproductive skew may be markedly affected by life history and natural history traits of the particular species and genera