Hynek Burda

Are naked and common mole-rats eusocial and if so, why?

Abstract Eusociality in mammals is defined in the present paper by the following criteria: reproductive altruism (which involves reproductive division of labor and cooperative alloparental brood care), overlap of adult generations, and permanent (lifelong) philopatry. We argue that additional criteria such as the existence of castes, colony size, reproductive skew, and social cohesion are not pertinent to the definition of eusociality in mammals. According to our definition of mammalian eusociality, several rodent species of the African family Bathyergidae can be considered eusocial, including the naked mole-rat (Heterocephalus glaber), Damaraland mole-rat (Cryptomys damarensis), and several additional, if not all, species in the genus Cryptomys. Furthermore, some species of social voles (like Microtus ochrogaster) may also fulfill criteria of mammalian eusociality. Understanding the evolution of eusociality in mole-rats requires answers to two primary questions: (1) What are the preconditions for the development of their eusocial systems? (2) Why do offspring remain in the natal group rather than dispersing and reproducing? Eusociality in mammals is by definition a special case of monogamy (more specifically: monogyny one female breeding), involving prolonged pair bonding for more than one breeding period. We argue that eusociality in mole-rats evolved from a monogamous mating system where cooperative brood care was already established. A tendency for group living is considered to be an ancestral (plesiomorph) trait among African bathyergid mole-rats, linking them to other hystricognath rodents. A solitary lifestyle seen in some genera, such as Bathyergus, Georychus, and Heliophobius, is assumed to be a derived trait that arose independently in different lineages of bathyergids, possibly as a consequence of selective constraints associated with the subterranean environment. In proximate terms, in eusocial mole-rats either puberty is assumed to be developmentally delayed so that under natural conditions most animals die before dispersal is triggered (e.g., in the case of Heterocephalus) or dispersal is induced only by an incidental encounter with an unfamiliar, yet adequate sexual partner (e.g., in the case of Cryptomys). Ultimately, a combination of strategies involving either dispersal and/or philopatry can be beneficial, especially in a highly unpredictable environment. If genetic relatedness among siblings is high (e.g., a coefficient of relatedness of 0.5 or more), then philopatry would not invoke an appreciable loss of fitness, especially if the cost of dispersing is higher than staying within the natal group. High genetic relatedness is more likely in a monogamous mating system or a highly inbred population. In this paper, we argue that the preconditions for eusociality in bathyergid mole-rats were a monogamous mating system and high genetic relatedness among individuals. We argue against the aridity food-distribution hypothesis (AFDH) that suggests a causal relationship between cooperative foraging for patchily distributed resources and the origin of eusociality. The AFDH may explain group size dynamics of social mole-rats as a function of the distribution and availability of resources but it is inadequate to explain the formation of eusocial societies of mole-rats, especially with respect to providing preconditions conducive for the emergence of eusociality.

A MAGNETIC POLARITY COMPASS FOR DIRECTION FINDING IN A SUBTERRANEAN MAMMAL

Correspondence to: S. Marhold While magnetic compass orientation in diverse representatives of birds, reptiles, amphibians, fishes, and insects has been intensively studied over the past three decades, in mammals it is poorly understood (e.g., compared to birds) and most of the evidence is still controversial [1]. The research in nonmammalian classes has focused mainly upon determining the global position and orientation by magnetic cues [2, 3] and examining the biophysical and neuronal features and constraints of magnetic compass orientation, with the ultimate goal of revealing the sensory and neuronal basis of the magnetic perception. On the other hand, studies in mammals are still at the stage of determining whether mammals have a magnetic compass [1]. Most of the earlier evidence was negative or, if positive, not conclusive. The problem in all of these studies was both methodological and the lack of a spontaneous directional behavior in a suitable animal. Experiments were designed to test the ability of mammals either to find a homeward direction when displaced [4] or tested in a circular arena [5] or to be trained to move in a certain direction, for example, to find food [6]. The results of those experiments were problematical because of the difficulty of removing other sensory cues or the lack of motivation, or because the magnetic compass orientation was tested out of its natural context. In addition, the experiments were performed indirectly, i.e., the magnetic field was artificially changed before (e.g., while transported to the release site or the test arena) rather than during the test. A few years ago we found a suitable way in which to investigate a possible magnetic compass in Zambian Gray’s common mole-rats,Cryptomys spp. These animals are small rodents of the family Bathyergidae with a body mass of about 100 g, which, as their more popular relatives, the naked mole-rats, live socially in large family groups (up to about 25 animals) underground. In our earlier study [7] we demonstrated that these subterranean mole-rats housed in a circular arena prefer to build their nests in its southeastern sector, and that they change their directional preference if the magnetic field is shifted by means of Helmholtz coils. Two sibling species of Cryptomysfrom Zambia were involved in our recent experiments: mole-rats originating from the Lusaka area with a karyotype 2n=68 [8] and mole-rats from Itezhi-Tezhi (Kafue National Park) with a karyotype 2n=58. (We have referred to the 2n=68 species as to C. hottentotusin our earlier papers, but later it emerged that both groups are new and as far unnamed species [9].) The experimental design was described in detail previously [7]. In brief, the animals (all members of one family group) were released in groups in a circular arena (diameter 82 cm) with a scattered nest material (slips of tissue papers, etc.). The animals gathered the material and within one to few hours built a nest, the position of which was recorded. The magnetic field conditions were manipulated by Helmholtz coils. The various experimental trials and control trials alternated in an irregular fashion. The northern direction and inclination were measured by means of a special inclination compass. Total intensities of the various magnetic field conditions were controlled by a calibrated gauss meter (Bell, Orlando, mod. 640 and MAG 01, Bartington). Light intensity inside the arena was determined by a calibrated luxmeter (United Detector, Santa Monica CA, model UDT-111A) in four compass directions and perpendicular from bottom to top. The following experiments were carried out in a wooden cottage far enough from other buildings (e.g., the animal house) with respect to the natural magnetic field conditions. The exact results and statistics are provided in Figs. 1–3.

Magnetic alignment in grazing and resting cattle and deer

We demonstrate by means of simple, noninvasive methods (analysis of satellite images, field observations, and measuring “deer beds” in snow) that domestic cattle (n = 8,510 in 308 pastures) across the globe, and grazing and resting red and roe deer (n = 2,974 at 241 localities), align their body axes in roughly a north–south direction. Direct observations of roe deer revealed that animals orient their heads northward when grazing or resting. Amazingly, this ubiquitous phenomenon does not seem to have been noticed by herdsmen, ranchers, or hunters. Because wind and light conditions could be excluded as a common denominator determining the body axis orientation, magnetic alignment is the most parsimonious explanation. To test the hypothesis that cattle orient their body axes along the field lines of the Earths magnetic field, we analyzed the body orientation of cattle from localities with high magnetic declination. Here, magnetic north was a better predictor than geographic north. This study reveals the magnetic alignment in large mammals based on statistically sufficient sample sizes. Our findings open horizons for the study of magnetoreception in general and are of potential significance for applied ethology (husbandry, animal welfare). They challenge neuroscientists and biophysics to explain the proximate mechanisms.

Subterranean Rodents: News from Underground

Across the globe, in all continents but Australia and Antarctica, at least 250 extant rodent species (38 genera, 6 families – according to the classification applied) spend most of their lives in self-constructed burrows (Table 1.1, Fig. 1.1). Their subterranean ecotope is dark, microclimatically stable, hypoxic and hypercapnic, and deprived of most sensory cues available aboveground. The burrows offer shelter from predators and climatic extremes, but digging is energetically costly, and the yield of foraging is relatively low, because the productivity of the subterranean ecotope is rather low and the food resources (roots and underground plant storage organs like bulbs and tubers) are mostly unpredictably and unevenly scattered. These so-called subterranean rodents are specialized in multiple aspects for their unique way of life in which most events like foraging, mating, and breeding take place underground. Animals that inhabit underground selfmade tunnels, but also forage (predominantly) above ground, are called fossorial. Needless to say, a continuum exists between fossorial and subterranean rodents, and in the present volume a categorical differentiation is mostly ignored on purpose. Another mammalian group sharing the same ecotope, but feeding on invertebrates, are subterranean non-rodent mammals likemarsupial moles, certain armadillos, as well as “insectivore” moles (e.g. Talpidae) and golden moles (Chrysochloridae). Although the title of the book emphasizes that the focus is on subterranean rodents, we also encouraged the authors to glance at recent findings from studies on other subterraneanmammals, and we hope that the reader will profit from this. Most subterranean rodent taxa have already been scientifically described in the golden ages of alpha taxonomy 100–200 years ago (and, e.g. the blind mole-rat Spalax and the mole-vole Ellobius talpinus in 1770), and many subterranean dwellers have been familiar to local people for ages (Spalax

Extremely low-frequency electromagnetic fields disrupt magnetic alignment of ruminants

Resting and grazing cattle and deer tend to align their body axes in the geomagnetic North-South direction. The mechanism(s) that underlie this behavior remain unknown. Here, we show that extremely low-frequency magnetic fields (ELFMFs) generated by high-voltage power lines disrupt alignment of the bodies of these animals with the geomagnetic field. Body orientation of cattle and roe deer was random on pastures under or near power lines. Moreover, cattle exposed to various magnetic fields directly beneath or in the vicinity of power lines trending in various magnetic directions exhibited distinct patterns of alignment. The disturbing effect of the ELFMFs on body alignment diminished with the distance from conductors. These findings constitute evidence for magnetic sensation in large mammals as well as evidence of an overt behavioral reaction to weak ELFMFs in vertebrates. The demonstrated reaction to weak ELFMFs implies effects at the cellular and molecular levels.

The magnetic compass mechanisms of birds and rodents are based on different physical principles

Recently, oscillating magnetic fields in the MHz-range were introduced as a useful diagnostic tool to identify the mechanism underlying magnetoreception. The effect of very weak high-frequency fields on the orientation of migratory birds indicates that the avian magnetic compass is based on a radical pair mechanism. To analyse the nature of the magnetic compass of mammals, we tested rodents, Ansells mole-rats, using their tendency to build their nests in the southern part of the arena as a criterion whether or not they could orient. In contrast to birds, their orientation was not disrupted when a broad-band field of 0.1–10 MHz of 85 nT or a 1.315 MHz field of 480 nT was added to the static geomagnetic field of 46 000 nT. Even increasing the intensity of the 1.315 MHz field (Zeeman frequency in the local geomagnetic field) to 4800 nT, more than a tenth of the static field, the mole-rats remained unaffected and continued to build their nests in the south. These results indicate that in contrast to that of birds, their magnetic compass does not involve radical pair processes; it seems to be based on a fundamentally different principle, which probably involves magnetite.

Individual recognition and incest avoidance in eusocial common mole-rats rather than reproductive suppression by parents

Non-reproductive females in families of eusocial common mole-rats (Cryptomys sp., Rodentia) are not suppressed by their mother, (either behaviourally or pheromonally) as is generally assumed. They do not mate with their father and brothers simply because they are not sexually attractive for them (and vice versa). The incest avoidance is based on the capability to recognize (and keep in memory for up to three weeks) each family member individually. A ‘sterile’ daughter may conceive and deliver young in her parental family if given the opportunity to mate with an unfamiliar mate in a separate cage. In this way, two females may breed side by side in one family.

Unusual cone and rod properties in subterranean African mole-rats (Rodentia, Bathyergidae)

We have determined the presence of spectral cone types, and the population densities of cones and rods, in subterranean mole‐rats of the rodent family Bathyergidae, for which light and vision seems of little importance. Most mammals have two spectral cone types, a majority of middle‐ to long‐wave‐sensitive (L‐) cones, and a minority of short‐wave‐sensitive (S‐)cones. We were interested to see whether the subterranean bathyergids show the same pattern. In three species, Ansells mole‐rat Cryptomys anselli, the giant mole‐rat Cryptomys mechowi and the naked mole‐rat Heterocephalus glaber, spectral cone types and rods were assessed immunocytochemically with opsin‐specific antibodies. All three species had rod‐dominated retinae but possessed significant cone populations. A quantitative assessment in C. anselli and C. mechowi revealed surprisingly low photoreceptor densities of 100 000–150 000/mm2, and high cone proportions, ≈ 10% (8000–15 000/mm2). In all three species, the vast majority of the cones were strongly S‐opsin‐immunoreactive; L‐opsin immunoreactivity was much fainter. In C. anselli, ≈ 20% of the cones showed exclusive S‐opsin label, ≈ 10% exclusive L‐opsin label and ≈ 70% strong S‐opsin and faint L‐opsin double label (potential dual‐pigment cones). This is the first observation in any mammal of an S‐opsin dominance and low levels of L‐opsin across the entire retina. It contrasts starkly with the situation in the muroid blind mole‐rat Spalax ehrenbergi, which has been reported to possess L‐opsin but no S‐opsin. Evidently, within rodents an adaptation to subterranean life is compatible with very different spectral cone properties.

Silvery mole-rats (Heliophobius argenteocinereus, Bathyergidae) change their burrow architecture seasonally

Little is known about seasonal changes in burrowing activity and burrow architecture in subterranean African mole-rats (Bathyergidae, Rodentia). The solitary genus Heliophobius is the least known genus of this family. We examined burrow systems of the silvery mole-rat (Heliophobius argenteocinereus) in Malawi in two periods of the dry season. Burrow pattern was influenced by the time of the year, becoming more reticulated at the peak of the dry season when soil was dry and hard. Overall digging activity did not cease during the dry season; yet burrowing strategy changed and the soil was deposited in tunnels rather than transported to mounds. The length of burrow systems was correlated with the body mass of the respective occupants. In spite of their solitary habits – and contrary to the prediction of the aridity food-distribution hypothesis – silvery mole-rats are able to occupy poor habitats with low food supply.

Sexual activity and reproduction delay ageing in a mammal

A trade-off between fecundity and life expectancy is fundamental to most theories on the evolution of life histories and ageing. In fact, sexual reproduction has been shown to reduce lifespan in a large number of species across all biological taxa [1]. The only exception known thus far are eusocial hymenopterans, with reproducing queens usually living much longer than the sterile workers [2]. Here, we show that in a eusocial mammal, a nearly identical life history has evolved.