Andreas Scharff

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.

NATURAL HISTORY OF THE GIANT MOLE-RAT, CRYPTOMYS MECHOWI (RODENTIA: BATHYERGIDAE), FROM ZAMBIA

Abstract We present the 1st detailed field study on the giant mole-rat (Cryptomys mechowi), a eusocial subterranean bathyergid rodent from mesic areas of subequatorial central Africa. In Copperbelt Province, Zambia, we found giant mole-rats in a variety of habitats including agricultural fields, bushland, marshes, and forests. Soil types varied in hardness and air content, and varied vertically and horizontally. Burrow systems of single colonies were 0.2–2.5 ha. The diameter of burrows was about 8 cm, and the maximum depth was about 200 cm. Nests were found at an average depth of 91 cm (n = 8). Further characteristics of nests, food and defecation chambers, diet, helminth parasites, and commensals are described. Colony size ranged from 3 to >20 with a sex ratio of 1:1.2 (n = 65) in favor of females, with 8% juveniles, 39% subadults, and 53% adults. A significant sexual dimorphism was found in the body mass (345 g ± 95 SD in males versus 252 ± 34 g in females). A defined breeding season was not apparent. Because C. mechowi occurs in a variety of habitats across a broad geographic range, generalizations based on the examination of selected study sites and consequent linking of behavioral ecology with habitat parameters should be done with caution.

Emmonsiosis of subterranean rodents (Bathyergidae, Spalacidae) in Africa and Israel

The presence of adiaspores of the fungal genus Emmonsia was examined in the lungs of 85 mole rats representing 3 subterranean genera: blind mole rats (Spalax galili and S. golani) from Israel, Ansells mole-rats (Cryptomys anselli) from Zambia, and silvery mole-rats (Heliophobius argenteocinereus) from Malawi and Zambia. Emmonsiosis was found in 28% of the blind mole rats, 100% of the Ansells mole-rats, but in none of the silvery mole-rats. Infection in African mole-rats was caused by Emmonsia parva, and infection in Israeli blind mole rats was caused by E. parva and E. crescens. The study indicates that the perennial burrow system of the Ansells mole-rat forms an appropriate microhabitat for the saprophytic growth of E. parva in Lusaka region, Zambia. We suggest that factors contributing to the striking difference in prevalence of emmonsiosis between the two African mole-rat genera (Cryptomys, Heliophobius) may be their differing burrow types, burrow longevity, and social lives.

Eusociality, life underground and parasites

In their recent review, Wcislo and Danforthl provided evidence of a secondary loss of social behaviour in halictid and apid bees. Their unorthodox view may help to illuminate the evolution of social behaviour in other organisms or will, at least, provide a new stimulus for discussion. One of their conclusions was that the maintenance of eusocial behaviour might be too costly because of an increased likelihood of disease and parasite transmission. However, very little was said about this in the reference2 cited by the authors to support their argument. It would be interesting to know what the evidence really is for increased risks of being parasitized in eusocial bees compared with their solitary relatives. Recently, we have shown3 that very similar arguments to those of Wcislo and Danforth may also apply to the evolution of sociality (or solitariness) in African bathyergid mole-rats (Cryptomys and Heliophobius). We examined the incidence of parasites in the eusocial Cr/ptOmyS genus”. As pointed out by Alexander et a/.2, most eusocial forms live in the soil and these mole-rats are no exception. The ecotope is humid and warm5 and, combined with social behaviour (such as close contact, communal toilets and coprophagy), would be expected to favour diseases and parasites. However, compared with some above-ground and burrowing small mammal@, which are usually infested by ectoand endoparasites, Cryptomys species are virtually ectoparasite-free and are much less infested with helminths [usually only with the nematode Protospirura muricola)4. Although the related, but solitary, silvery mole-rat, Heliophobius, seems to be even less infected than Cfyptomys (A. Scharff and H. Burda, unpublished), the blind mole-rat, Spalax ehrenbergi, which is also solitary and subterranean, shows high infestation rates with nematodes’. These data are confusing. On the one hand, the data on bathyergids suggest that the subterranean lifestyle reduces the likelihood of parasitic infechons and that this risk is further lowered by a solitary lifestyle; this would support the hypothesis of Wcislo and Danforthl. On the other hand, Spalax infestation rates do not differ from those of other small rodents. Unfortunately, because there are still too few comparative data and very little is known about the life cycles and requirements of helminth parasites, these inconsistencies and, therefore, the relationship between parasites, the subterranean way of life and social behaviour in mole-rats will remain unexplained.