Growth and development in six species of African mole-rats (Rodentia: Bathyergidae)

The bathyergid mole-rats provide a unique example of a family of subterranean rodents exhibiting a broad spectrum of sociality. Three genera comprise solitary, strongly territorial individuals whereas two genera are social. This sociality culminates in the eusocial naked mole-rat, Heterocephalus glaber . The pups of solitary mole-rats disperse, establish and thereafter defend their own burrow systems when approximately two months old, whereas those of social genera join an established natal colony. This paper examines whether these different lifestyles are reflected in the early development and rate of growth of pups of mole-rats.
Although the trends are not clear-cut, it is apparent that the pups of solitary genera grow and mature more rapidly than those from social genera. Thus, the growth rate constant ( K ) for the first70–80 days of postnatal growth (using the Gompertz equation) for the solitary genera was between 0.042 and 0.052 day⁻¹, whereas that of the social mole-rats was considerably lower (0.01 5 day⁻¹). Similarly the mean growth rates of solitary genera ranged between 3.3 and 1.227g/day while those of the social mole-rats were 0.229-0.233 g/day.
The pattern of development and the rates of growth in solitary bathyergids are similar to those of other solitary subterranean rodents. One interesting feature common to all the social genera studied to date was that the first pups recruited to a 'new colony', consisting of a reproductive pair of adult mole-rats, grew at a significantly faster rate than pups born to an established colony.     

Phylogeographical patterns of genetic divergence and speciation in African mole-rats (Family: Bathyergidae)

African mole-rats are subterranean Hystricomorph rodents, distributed widely throughout sub-Saharan Africa, and displaying a range of social and reproductive strategies from solitary dwelling to the 'insect-like' sociality of the naked mole-rat, Heterocephalus glaber. Both molecular systematic studies of Rodentia and the fossil record of bathyergids indicate an ancient origin for the family. This study uses an extensive molecular phylogeny and mitochondrial cytochrome b and 12s rRNA molecular clocks to examine in detail the divergence times, and patterns of speciation of the five extant genera in the context of rift valley formation in Africa. Based on a value of 40-48 million years ago (Myr) for the basal divergence of the family (Heterocephalus), we estimate divergence times of 32-40 Myr for Heliophobius, 20-26 Myr for Georychus/Bathyergus and 12-17 Myr for Cryptomys, the most speciose genus. While early divergences may have been independent of rifting, patterns of distribution of later lineages may have been influenced directly by physical barriers imposed by the formation of the Kenya and Western Rift, and indirectly by accompanying climatic and vegetative changes. Rates of chromosomal evolution and speciation appear to vary markedly within the family. In particular, the genus Cryptomys appears to have undergone an extensive radiation and shows the widest geographical distribution. Of the two distinct clades within this genus, one exhibits considerable karyotypic variation while the other does not, despite comparatively high levels of sequence divergence between some taxa. These different patterns of speciation observed both within the family and within the genus Cryptomys may have been a result of environmental changes associated with rifting.     

Circadian rhythms of locomotor activity in Drosophila

Drosophila is by far the most advanced model to understand the complex biochemical interactions upon which circadian clocks rely. Most of the genes that have been characterized so far were isolated through genetic screens using the locomotor activity rhythms of the adults as a circadian output. In addition, new techniques are available to deregulate gene expression in specific cells, allowing to analyze the growing number of developmental genes that also play a role as clock genes. However, one of the major challenges in circadian biology remains to properly interpret complex behavioral data and use them to fuel molecular models. This review tries to describe the problems that clockwatchers have to face when using Drosophila activity rhythms to understand the multiple facets of circadian function.     

Circadian rhythms of self-feeding and locomotor activity in zebrafish (Danio Rerio)

To investigate daily feeding rhythms in zebrafish, the authors have developed a new self-feeding system with an infrared photocell acting as a food-demand sensor, which lets small-size fish such as zebrafish trigger a self-feeder. In this paper, the authors used eight groups of 20 fish. Locomotor activity rhythms were also investigated by means of infrared sensors. Under a 12?h:12?h light (L)-dark (D) cycle, zebrafish showed a clear nocturnal feeding pattern (88.0% of the total daily food-demands occurring in the dark phase), concentrated during the last 4?h of the dark phase. In contrast, locomotor activity was mostly diurnal (88.2% of total daily activity occurring in the light phase). Moreover, both feeding and locomotor rhythms were endogenously driven, as they persisted under free-running conditions. The average period length (τ) of the locomotor and feeding rhythms was shorter (τ?=?22.9?h) and longer (τ?=?24.6?h) than 24?h, respectively. During the time that food availability was restricted, fish could only feed during ZT0-ZT12 or ZT12-ZT16. This resulted in feeding activity being significantly modified according to feeding time, whereas the locomotor activity pattern remained synchronized to the LD cycle and did not change during this trial. These findings revealed an independent phasing between locomotor and feeding activities (which were mostly nocturnal or diurnal, respectively), thus supporting the concept of multioscillatory control of circadian rhythmicity in zebrafish.     

Hind foot drumming: Morphofunctional analysis of the hind limb osteology in three species of African mole-rats (Bathyergidae)

Hind foot drumming is a form of seismic signaling that plays a vital role in the communication of several Bathyergidae species. Hind foot drumming is initiated by the rapid movement of the whole hind limb by flexion and extension of the hip and knee. This study aimed to determine if morphological adaptations of the hind limb osteology were measurable using established morphometric analyses in two drumming (Bathyergus suillus and Georychus capensis) and one non-drumming (Cryptomys hottentotus natalensis) African mole-rat species. Forty-three linear measurements of the hind limb were taken in 48 limbs (n = 16 limbs per species) and 32 indices were calculated. Mixed model analysis of variance was used to compare the three species and sexes within a species. Thirteen indices had significant differences between species. Eleven indices had significant differences between sexes within a species. Significant differences between the drumming (B. suillus and G. capensis) and the non-drumming species were observed in three indices. The femoral greater trochanter was relatively shorter in the drumming species compared to the non-drumming species, which is proposed to allow for increased hip joint mobility, thereby permitting drummers to move their limbs at the rapid speed required to generate seismic signals. Furthermore, the small in-lever (shorter greater trochanter) may increase the velocity of limb motion. The robust tibias in the drumming species, as indicated by the tibial robustness index, are likely to counter the additional biomechanical load caused by the muscles involved in hind foot drumming. The relatively small hind feet seen in the drumming species allows for reduced limb weight needed for the rapid extension and flexion motion required during hind foot drumming. The significant differences reflected in the hind limb osteological indices between B. suillus and G. capensis and the non-drumming species are indicative of adaptations for hind foot drumming.     

Parasites in social subterranean Zambian mole-rats (Cryptomys spp., Bathyergidae, Rodentia)

Three out of 18 examined common mole-rats ( Cryptomys sp., Xkaryotype 2n = 58) from Zambia were infested with cestodes ( Inermicapsifer nmdagascariensis and an undetermined species) and a nematode ( Protospirura muricola ). Four out of 14 examined Zambian giant mole-rats ( Cryptomys mechowi ) hosted cestodes ( Raillietina (R) sp. and an undetermined species) and nematodes ( Protospirura muricola, Capillaria sp.). Helminths and circumstances of findings are briefly described. No ectoparasites were found. The influences of subterranean and social way of life and feeding habits upon occurrence of parasites in mole-rats are discussed. Burrow conditions and social behaviour seem not to favour infestation by parasites.     

Patterns of MHC selection in African mole-rats, family Bathyergidae: the effects of sociality and habitat

African mole-rats are a family of rodents exhibiting an eclectic range of social behaviour and occupying a variety of habitat types. These differences are likely to impact upon the risk of parasite transmission and virulence, with increasing sociality predicted to correspond to an increased risk of transmission. We investigate these factors by analysing the major histocompatibility complex (MHC), a set of genes responsible for encoding highly variable intermediaries of the vertebrate adaptive immune response. To this end we assessed selection at exons 2 and 3 of the MHC class II DQalpha1 gene of four African mole-rat species representing a range of social behaviours. We demonstrate that: (i) the overall pattern of selection at these exons differentiates according to the predicted function of different regions, with the presence of positive selection indicating the likely influence of host-parasite coevolution; and (ii) contrary to the often observed and predicted positive correspondence between sociality and the risk of parasite transmission, two highly social African mole-rat species in fact appear to have comparatively weak positive selection, suggesting diminished host immunity and thus a low overall risk of parasite transmission.     

Circadian rhythms of demand-feeding and locomotor activity in rainbow trout

Under free-running conditions, most rainbow trout displayed circadian feeding rhythms, although the expression of circadian rhythmicity depended on the experimental condition: 16·7% of fish under constant dim light (LL dim), 66·1% under a 45 :45 min light-dark cycle (LD pulses), and 83·8% under constant light (LL). Under LD pulses, the period length of the free-running rhythms for feeding was significantly shorter (21·9 ± 0·7 h, n =8) than under LL (26·2 ± 0·3 h, n =10). Period length for locomotor activity under LL was 25·8 ± 0·6 h ( n =4). Under LD conditions, the daily demand-feeding profile was always confined to the light phase and chiefly composed of two main episodes, directly after lights on (light elicited) and in anticipation to lights off (endogenous). Contrasting to feeding, the diel locomotor activity profile varied remarkably: a diurnal activity pattern at the bottom, while a clearly nocturnal pattern at the surface. These results contribute to a better understanding of feeding and locomotor rhythms of rainbow trout, providing evidence for the existence of a biological clock involved in their circadian control. This finding contrasts with the previously recorded lack of an endogenous oscillator in the pineal organ driving the rhythmic secretion of melatonin, which suggests different locations from the pineal for the circadian pacemakers in this species.     

Energetics in a solitary subterranean rodent, the silvery mole-rat, Heliophobius argenteocinereus, and allometry of RMR in African mole-rats (Bathyergidae)

Low resting metabolic rate (RMR) in subterranean rodents used to be considered as a physiological adaptation to cope with stresses of the belowground environment. In African mole-rats (Bathyergidae, Rodentia), RMR was reported to be independent of body mass. This deviation from a general mammalian pattern was considered a precondition for evolution of eusociality, occurring in some bathyergids. We measured metabolic rate and thermoregulation in the silvery mole-rat, Heliophobius argenteocinereus, the only bathyergid genus for which well-supported, comparable data were still missing. Low RMR (154.04 mL O(2) h(-1), which is 82% of the value predicted for a rodent) corresponds to the value expected in a subterranean rodent. Broad range of the thermoneutral zone (25-33 degrees C) and only slightly higher conductance (17.3 mL O(2) h(-1) degrees C(-1), i.e. 112.5% of that predicted for subterranean mammals) indicate that H. argenteocinereus is adapted to lower burrow temperatures rather than to high temperatures. Low RMR in this solitary species, as in other subterranean rodents in general, is probably associated particularly with high energetic cost of foraging. Our results combined with data on other mole-rats show clearly that RMR within the Bathyergidae is mass-dependent.     

Acoustic communication underground: vocalization characteristics in subterranean social mole-rats (Cryptomys sp., Bathyergidae)

In captive adult Zambian mole-rats 14 different sounds (13 true vocalizations) have been recorded during different behavioural contexts. The sound analysis revealed that all sounds occurred in a low and middle frequency range with main energy below 10 kHz. The majority of calls contained components of 1.6–2 kHz, 0.63–0.8 kHz, and/or 5–6.3 kHz. The vocalization range thus matched well the hearing range as established in other studies. The frequency content of courtship calls in two species of Zambian Cryptomys was compared with that in naked mole-rats (Heterocephalus glaber) and blind mole-rats (Spalax ehrenbergi) as described in the literature. The frequency range of maximum sound energy is negatively correlated with the body weight and coincides with the frequencies of best hearing in the respective species. In general, the vocalization range in subterranean mammals is shifted towards low frequencies which are best propagated in underground burrows. Accepted: 16 September 1996     

Thermal biology of a strictly subterranean mammalian family,the African mole-rats (Bathyergidae,Rodentia) - a review

African mole-rats are subterranean rodents, which rarely if ever leave the safety of their burrow systems. The environment of the burrows is humid, with relatively stable temperatures, and may have a hypoxic and hypercapnic atmosphere. One of crucial problems related to the subterranean way of life in mammals is avoidance of overheating, because traditional mammalian cooling mechanisms are not effective under high humidity. In African mole-rats, a variety of adaptations have evolved in response to this and other challenges of the underground ecotope. Traditionally, attention has been devoted mainly to the naked mole-rat Heterocephalus glaber, which became popular as a result of its eusociality and absence of fur, both being unique phenomena in small mammals. Despite more recent research, information on other species is still relatively limited and patchy. I review the results of studies on African mole-rats that are relevant for the understanding of their energetics and thermal biology. Attention is paid to the parameters of the burrow environment, which represent the main selection pressures shaping their physiology. In addition, an overview is given of the morphological, physiological and behavioural adaptations helping mole-rats to face temperature extremes, mechanisms by which they deal with a surplus of metabolic heat and how changes in ambient temperature influence their daily activity. The naked mole-rat is compared to its furred relatives to determine whether this species is really exceptional from the point of thermal biology. An ordination analysis was conducted using published data on mole-rat body temperature, thermoneutral zone, resting metabolic rate and thermal conductance. Most of the variability in these characteristics was found to be explained by body mass, followed by temperature characteristics of climate, but not precipitation, of the species distributional ranges. This analysis shows that the naked mole-rat is comparable to the other mole-rat species in these physiological characteristics.     

Circadian rhythms of locomotor activity in cockroach nymphs: free running and entrainment

The temporal organization of locomotor activity was investigated in nymphs of the cockroach Leucophaea maderae. Approximately 40% of the animals examined between 1 and 50 days of age exhibited a circadian activity rhythm in constant darkness (n = 172) with an average free-running period of 23.7 +/- 0.68 hr. Twelve of 17 animals in which activity was recorded for most or all of the final instar also exhibited periods of rhythmic activity. The rhythms of the nymphs could be entrained by light-dark (LD) cycles with periods of 22, 24, or 26 hr. In contrast, neither maternal influences during embryogenesis nor hatching from the egg was effective in synchronizing the rhythms. Although adult cockroaches can be readily entrained by temperature cycles, in nymphs temperature appeared at best to be a weak zeitgeber. Embryonic exposure to an LD cycle until 6 days prior to egg hatch was effective in synchronizing the activity rhythms of the nymphs, indicating that differentiation of an entrainable pacemaking system occurs prior to hatching.     

A tangled history: patterns of major histocompatibility complex evolution in the African mole-rats (Family: Bathyergidae)

Phylogenetic trees based upon major histocompatibility complex (MHC) gene sequences, particularly those encompassing sites encoding the antigen recognition site, are often discordant with the species tree. It has been argued that the principal cause of such discordance is the presence of ancestrally derived polymorphisms persisting through speciation events as a consequence of selection. In the present study, we examine the evolution of the MHC class II DQα1 gene in an unusual family of hystricomorph rodents, the African mole-rats (Family: Bathyergidae). We show that there is a high level of trans-species polymorphism and that this is a result of positive selection. Furthermore, the major lineages of the gene tree are characterized by allelic motifs occurring in regions that coincide with the pocket domains of the putative antigen recognition site, a region that has been shown to be under positive selection in a number of MHC genes from a range of species. Finally, these alleles may have been retained for at least 48 million years. This is significantly older than the estimate for the equivalent primate locus and appears to be one of the oldest documented sets of MHC alleles. We suggest that these allelic motifs possess polymorphisms that have been immunologically important to African mole-rats over long periods of evolutionary history.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 493–503.     

Coefficients of digestibility and nutritional values of geophytes and tubers eaten by southern African mole-rats (Rodentia: Bathyergidae)

Subterranean rodents have high energy requirements when they are excavating their burrows. This study investigates the energy available to, and the efficiency with which it can be extracted by, four species of bathyergid mole-rats fed natural diets ranging from the underground storage organs of geophytes to grass roots and leaves.
The digestibility coefficients of geophytes ranged from 53% for the fibrous tuber of the gemsbok cucumber to 95–7% for corms and bulbs. One species, Bathyergus suillus whose diet consists of over 80% grass, had a digestibility coefficient of 87% on an all grass diet.
All species had similar coefficients of digestibility of > 90% when fed on a uniform diet of sweet potato.
Bulbs and corms had a low fibre content (3–3–4%), high calorific value (15–16kJ/g) and high digestibility coefficients (95–7–96%) and on this diet the mole-rats maintained their body mass. Food of lower digestibility tended to have a high fibre content (8–2–45%) and, with the exception of B. suillus , although the mole-rats consumed a greater quantity of food, they lost mass. The sweet potato had a low fibre content (4–1 %) but was energetically very similar to bulbs and corms (15–5 kJ/g).
Geophytes which have low fibre contents are generally small (1–20 g), whereas geophytes with high fibre contents are much larger (30–2000 g) and often occur in more arid zones.     

Evidence from intron 1 of the nuclear transthyretin (Prealbumin) gene for the phylogeny of African mole-rats (Bathyergidae)

A 900- to 1100-bp fragment encompassing intron 1 of the nuclear transthyretin (prealbumin) gene was examined in 12 taxa of Old World hystricognath rodents of the families Bathyergidae, Petromuridae, Thryonomyidae, and Hystricidae. Within the Bathyergidae, Heterocephalus glaber (naked mole-rat) was basal, and the other East African species, Heliophobius argenteocinereus (silvery mole-rat), was sister to a southern African clade containing Bathyergus, Cryptomys, and Georychus (dune, common, and cape mole-rats). These results are congruent with studies using mitochondrial 12S rRNA gene sequences. A combined analysis of transthyretin and 12S rRNA data resulted in a well-supported topology with better resolution than either gene analyzed separately. These data support the findings by M. W. Allard and R. L. Honeycutt (1992, Mol. Biol. Evol. 9: 27-40) and R. L. Honeycutt (1992, Am. Sci. 80: 43-53) that complex social systems evolved independently at least twice, in the common and naked mole-rats.     

Thermoregulation in three species of Afrotropical subterranean mole-rats (Rodentia: Bathyergidae) from Zambia and Angola and scaling within the genus Cryptomys

The thermoregulatory characteristics of three species of Cryptomys from Zambia and Angola are examined and, together with published data on four other species of Cryptomys from southern Africa, used to determine whether scaling occurs in this genus of subterranean rodents. The thermoregulatory properties of acclimated giant Zambian mole-rats, Cryptomys mechowi ( =267 g), Angolan mole-rats, Cryptomys bocagei ( =94 g) and Zambian common mole-rats Cryptomys hottentotus amatus ( =77 g) are as follows. Mean resting metabolic rates (RMRs) within the respective thermoneutral zones were 0.60±0.08 cm³ O₂ g^-1 h^-1 (n=12) for C. mechowi; 0.74±0.06 cm³ O₂ g^-1 h^-1 (n=8) for C. bocagei and 0.63±0.06 cm³O₂ g^-1 h^-1 (n=21) for C. h. amatus. The thermoneutral zones (TNZs) of all three species are narrow: 29–30°C for C. mechowi; 31.5–32.5°C for C. bocagei and 28–32° C for C. h. amatus. The increase in mean RMR at the lowest temperatures tested (15° C for C. mechowi, 18° C for C. bocagei and C. h. amatus) was 2.35, 2.2 and 3.82 times their RMR in the TNZ respectively. Body temperatures are low, 34±0.53° C (n=24) for C. mechowi, 33.7±0.32° C (n=20) for C. bocagei and 33.8±0.43° C (n=40) for C. h amatus. At the lower limit of thermoneutrality, conductances are 0.09±0.01 cm³ O₂ g^-1 h^-1 °C^-1 (n=30) in C. mechowi; 0.12±0.01 cm³ O₂ g^-1 h^-1 °C^-1 (n=20) in C. bocagei and 0.12±0.03 cm³ O₂ g^-1 h^-1 °C^-1 (n=32) in C. h. amatus. The range in mean body mass among the seven species of Cryptomys examined for scaling was 60 g (C. darlingi) to 267 g (C. mechowi). There is no clear relationship between RMR within the TNZ and body mass. The resultant relationship is represented by the power curve RMR=2.45 mass^-0.259.