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1.
Int J Parasitol Parasites Wildl ; 24: 100950, 2024 Aug.
Article in English | MEDLINE | ID: mdl-38966857

ABSTRACT

Males and females in sexually dimorphic species show differences in their physiology and behaviour due to differences in energetic investment into reproduction and soma. This means that the two sexes may show different patterns of parasitism at different times of the year. In this study, we evaluate the abundance of fecal eggs and larvae of 5 parasite types (Strongyles, Nematodirus spp., Marshallagia marshalli., Protostrongylus spp. lungworms, and Eimeria spp.) in relation to season and sex in Rocky Mountain bighorn sheep (Ovis canadensis). We use fecal egg counts (FEC) as a proxy for infection intensity. Parasite FECs differed between male and female bighorn sheep and varied with season. We found pronounced fluctuations in fecal egg counts of various parasite species in males and females across different seasons and reproductive stages. Strongyle counts were significantly higher during late gestation and lactation/summer, and particularly pronounced in males. Nematodirus counts were highest during late gestation in females and during the rut in males. Marshallagia counts peaked during late gestation in females and during the rut in males. Protostrongylus spp. lungworm counts were highest during late gestation in females and in males during lactation/summer and the rut. Eimeria oocyst counts varied across seasons, with higher counts in males during the rut and in females during winter and late gestation. Additionally, significant differences in Strongyle counts were observed between coursing and tending rams, with tending rams exhibiting higher counts. We discuss why the sexes might differ in FECs and suggest that differences between FECs of the parasites across seasons may be due to different life cycles and cold tolerance of the parasites themselves.

2.
Behav Ecol ; 34(6): 979-991, 2023.
Article in English | MEDLINE | ID: mdl-37969548

ABSTRACT

In many social species, both the acquisition of dominance and the duration that individuals maintain their status are important determinants of breeding tenure and lifetime reproductive success. However, few studies have yet examined the extent and causes of variation in dominance tenure and the duration of breeding lifespans. Here, we investigate the processes that terminate dominance tenures and examine how they differ between the sexes in wild Kalahari meerkats (Suricata suricatta), a cooperative breeder where a dominant breeding pair produces most of the young recruited into each group. Mortality and displacement by resident subordinate competitors were important forms of dominance loss for both sexes. However, dominant males (but rarely females) were also at risk of takeovers by extra-group invading males. Dominant males also differed from dominant females in that they abandoned their group after the death of their breeding partner, when no other breeding opportunities were present, whereas dominant females that lost their partner remained and continued to breed in the same group. We show that a larger number of processes can terminate dominance tenure in males with the result that the average male tenure of breeding positions was shorter than that of females, which contributes to the reduced variance in the lifetime reproductive success in males compared to females. Our analysis suggests that sex differences in emigration and immigration may often have downstream consequences for sex differences in reproductive variance and for the selection pressures operating on females and males.

3.
Evol Lett ; 7(4): 203-215, 2023 Aug.
Article in English | MEDLINE | ID: mdl-37475748

ABSTRACT

In eusocial invertebrates and obligate cooperative breeders, successful reproduction is dependent on assistance from non-breeding group members. Although naked (Heterocephalus glaber) and Damaraland mole-rats (Fukomys damarensis) are often described as eusocial and their groups are suggested to resemble those of eusocial insects more closely than groups of any other vertebrate, the extent to which breeding individuals benefit from the assistance of non-breeding group members is unclear. Here we show that, in wild Damaraland mole-rats, prospective female breeders usually disperse and settle alone in new burrow systems where they show high survival rates and remain in good body condition-often for several years-before being joined by males. In contrast to many obligate cooperative vertebrates, pairs reproduced successfully without non-breeding helpers, and the breeding success of experimentally formed pairs was similar to that of larger, established groups. Though larger breeding groups recruited slightly more pups than smaller groups, adult survival was independent of group size and group size had mixed effects on the growth of non-breeders. Our results suggest that Damaraland mole-rats do not need groups to survive and that cooperative breeding in the species is not obligate as pairs can-and frequently do-reproduce without the assistance of helpers. While re-emphasizing the importance of ecological constraints on dispersal in social mole-rats, the mixed effects of group size in our study suggest that indirect benefits accrued through cooperative behavior may have played a less prominent role in the evolution of mole-rat group-living than previously thought.

4.
J Anim Ecol ; 92(9): 1730-1742, 2023 09.
Article in English | MEDLINE | ID: mdl-37365766

ABSTRACT

Behavioural plasticity can allow populations to adjust to environmental change when genetic evolution is too slow to keep pace. However, its constraints are not well understood. Personality is known to shape individual behaviour, but its relationship to behavioural plasticity is unclear. We studied the relationship between boldness and behavioural plasticity in response to wind conditions in wandering albatrosses (Diomedea exulans). We fitted multivariate hidden Markov models to an 11-year GPS dataset collected from 294 birds to examine whether the probability of transitioning between behavioural states (rest, prey search and travel) varied in response to wind, boldness and their interaction. We found that movement decisions varied with boldness, with bolder birds showing preferences for travel, and shyer birds showing preferences for search. For females, these effects depended on wind speed. In strong winds, which are optimal for movement, females increased time spent in travel, while in weaker winds, shyer individuals showed a slight preference for search, while bolder individuals maintained preference for travel. Our findings suggest that individual variation in behavioural plasticity may limit the capacity of bolder females to adjust to variable conditions and highlight the important role of behavioural plasticity in population responses to climate change.


Subject(s)
Feeding Behavior , Wind , Female , Animals , Feeding Behavior/physiology , Birds/physiology , Personality
5.
Elife ; 102021 04 12.
Article in English | MEDLINE | ID: mdl-33843584

ABSTRACT

In some mammals and many social insects, highly cooperative societies are characterized by reproductive division of labor, in which breeders and nonbreeders become behaviorally and morphologically distinct. While differences in behavior and growth between breeders and nonbreeders have been extensively described, little is known of their molecular underpinnings. Here, we investigate the consequences of breeding for skeletal morphology and gene regulation in highly cooperative Damaraland mole-rats. By experimentally assigning breeding 'queen' status versus nonbreeder status to age-matched littermates, we confirm that queens experience vertebral growth that likely confers advantages to fecundity. However, they also upregulate bone resorption pathways and show reductions in femoral mass, which predicts increased vulnerability to fracture. Together, our results show that, as in eusocial insects, reproductive division of labor in mole-rats leads to gene regulatory rewiring and extensive morphological plasticity. However, in mole-rats, concentrated reproduction is also accompanied by costs to bone strength.


Some social animals are highly cooperative creatures that live in tight-knit colonies. Bees and ants are perhaps the most well-known examples of social insects, while Damaraland mole-rats and naked mole-rats, two rodent species found in southern and eastern Africa, are among the most cooperative mammal species. In these colony-forming animals, only one or a few females reproduce and these fertile females are frequently referred to as "queens". When an animal becomes a queen, her body shape can change dramatically to support the demands of high fertility and frequent reproduction. The molecular basis of such changes has been well-described in social insects. However, they are poorly understood in mammals. To address this knowledge gap, Johnston et al. studied how transitioning to queen status affects bone growth and structural integrity in Damaraland mole-rats, as well as body shape and size. The experiments compared non-breeding female mole-rats with other adult females recently paired with a male to become the sole breeder of a new colony. Johnston et al. also used bone-derived cells grown in the laboratory to assess underlying gene regulatory changes in new queen mole-rats. Johnston et al. showed that transitioning to the role of queen leads to a cascade of skeletal changes accompanied by shifts in the regulation of genetic pathways linked to bone growth. Queen mole-rats show accelerated growth in the spinal column of their lower back. These bones are called lumbar vertebrae and this likely allows them to have larger litters. However, queen mole-rats also lose bone growth potential in their leg bones and develop thinner thigh bones, which may increase the risk of bone fracture. Therefore, unlike highly social insects, mole-rats do not seem to have escaped the physical costs of intensive reproduction. This work adds to our understanding of the genes and physical traits that have evolved to support cooperative behaviour in social animals, including differences between insects and mammals. It also shows, with a striking example, how an animal's genome responds to social cues to produce a diverse range of traits that reflect their designated social role.


Subject(s)
Biological Evolution , Bone Development , Femur/growth & development , Fertility , Genome , Lumbar Vertebrae/growth & development , Mole Rats/growth & development , Sexual Behavior, Animal , Age Factors , Animals , Bone Development/genetics , Cooperative Behavior , Fertility/genetics , Gene Expression Regulation , Mole Rats/genetics , Mole Rats/psychology , Sex Factors , Social Behavior
6.
Biol Lett ; 16(10): 20200475, 2020 10.
Article in English | MEDLINE | ID: mdl-33023382

ABSTRACT

Eusocial societies are characterized by a clear division of labour between non-breeding workers and breeding queens, and queens often do not contribute to foraging, defence and other maintenance tasks. It has been suggested that the structure and organization of social mole-rat groups resembles that of eusocial insect societies. However, the division of labour has rarely been investigated in wild mole-rats, and it is unknown whether breeders show decreased foraging activity compared with non-breeding helpers in natural groups. Here, we show that, in wild Damaraland mole-rats (Fukomys damarensis), breeders show lower activity in foraging areas than non-breeding group members. Both breeders and non-breeders displayed variation in activity across the different seasons. Our results suggest that group living allows social mole-rat breeders to reduce their investment in energetically costly behaviour, or alternatively, that the high cost of reproduction in this species forces a behavioural trade-off against foraging investment.


Subject(s)
Mole Rats , Reproduction , Animals , Seasons
7.
PeerJ ; 8: e9214, 2020.
Article in English | MEDLINE | ID: mdl-32477839

ABSTRACT

Recent comparative studies have suggested that cooperative breeding is associated with increases in maximum lifespan among mammals, replicating a pattern also seen in birds and insects. In this study, we re-examine the case for increased lifespan in mammalian cooperative breeders by analysing a large dataset of maximum longevity records. We did not find any consistent, strong evidence that cooperative breeders have longer lifespans than other mammals after having controlled for variation in body mass, mode of life and data quality. The only possible exception to this general trend is found in the African mole-rats (the Bathyergid family), where all members are relatively long-lived, but where the social, cooperatively breeding species appear to be much longer-lived than the solitary species. However, solitary mole-rat species have rarely been kept in captivity or followed longitudinally in the wild and so it seems likely that their maximum lifespan has been underestimated when compared to the highly researched social species. Although few subterranean mammals have received much attention in a captive or wild setting, current data instead supports a causal role of subterranean living on lifespan extension in mammals.

8.
Mol Ecol ; 29(19): 3578-3592, 2020 10.
Article in English | MEDLINE | ID: mdl-32416000

ABSTRACT

Small population sizes can, over time, put species at risk due to the loss of genetic variation and the deleterious effects of inbreeding. Losing diversity in the major histocompatibility complex (MHC) could be particularly harmful, given its key role in the immune system. Here, we assess MHC class I (MHC-I) diversity and its effects on mate choice and survival in the Critically Endangered Raso lark Alauda razae, a species restricted to the 7 km2 islet of Raso, Cape Verde, since ~1460, whose population size has dropped as low as 20 pairs. Exhaustively genotyping 122 individuals, we find no effect of MHC-I genotype/diversity on mate choice or survival. However, we demonstrate that MHC-I diversity has been maintained through extreme bottlenecks by retention of a high number of gene copies (at least 14), aided by cosegregation of multiple haplotypes comprising 2-8 linked MHC-I loci. Within-locus homozygosity is high, contributing to low population-wide diversity. Conversely, each individual had comparably many alleles, 6-16 (average 11), and the large and divergent haplotypes occur at high frequency in the population, resulting in high within-individual MHC-I diversity. This functional immune gene diversity will be of critical importance for this highly threatened species' adaptive potential.


Subject(s)
Genetic Variation , Major Histocompatibility Complex , Alleles , Animals , Gene Dosage , Humans , Inbreeding , Islands , Major Histocompatibility Complex/genetics
9.
J Anim Ecol ; 89(4): 1080-1093, 2020 04.
Article in English | MEDLINE | ID: mdl-31943191

ABSTRACT

Researchers studying mammals have frequently interpreted earlier or faster rates of ageing in males as resulting from polygyny and the associated higher costs of reproductive competition. Yet, few studies conducted on wild populations have compared sex-specific senescence trajectories outside of polygynous species, making it difficult to make generalized inferences on the role of reproductive competition in driving senescence, particularly when other differences between males and females might also contribute to sex-specific changes in performance across lifespan. Here, we examine age-related variation in body mass, reproductive output and survival in dominant male and female meerkats, Suricata suricatta. Meerkats are socially monogamous cooperative breeders where a single dominant pair virtually monopolizes reproduction in each group and subordinate group members help to rear offspring produced by breeders. In contrast to many polygynous societies, we find that neither the onset nor the rate of senescence in body mass or reproductive output shows clear differences between males and females. Both sexes also display similar patterns of age-related survival across lifespan, but unlike most wild vertebrates, survival senescence (increases in annual mortality with rising age) was absent in dominants of both sexes, and as a result, the fitness costs of senescence were entirely attributable to declines in reproductive output from mid- to late-life. We suggest that the potential for intrasexual competition to increase rates of senescence in females-who are hormonally masculinized and frequently aggressive-is offset by their ability to maintain longer tenures of dominance than males, and that these processes when combined lead to similar patterns of senescence in both sexes. Our results stress the need to consider the form and intensity of sexual competition as well as other sex-specific features of life history when investigating the operation of senescence in wild populations.


Subject(s)
Herpestidae , Aging , Animals , Breeding , Female , Longevity , Male , Reproduction , Sexual Behavior, Animal
10.
Nat Hum Behav ; 3(8): 792-796, 2019 08.
Article in English | MEDLINE | ID: mdl-31110340

ABSTRACT

A long-standing hypothesis suggests that the transition from hunting and gathering to agriculture results in people working harder, spending more time engaged in subsistence activities and having less leisure time1,2. However, tests of this hypothesis are obscured by comparing between populations that vary in ecology and social organization, as well as subsistence3-6. Here we test this hypothesis by examining adult time allocation among the Agta-a population of small-scale hunter-gatherers from the northern Philippines who are increasingly engaged in agriculture and other non-foraging work. We find that individuals in camps engaging more in non-foraging work spend more time involved in out-of-camp work and have substantially less leisure time. This difference is largely driven by changes in the time allocation of women, who spend substantially more time engaged in out-of-camp work in more agricultural camps. Our results support the hypothesis that hunting and gathering allows a significant amount of leisure time, and that this is lost as communities adopt small-scale agriculture.


Subject(s)
Agriculture , Appetitive Behavior , Leisure Activities , Work , Adolescent , Adult , Age Factors , Aged , Anthropology, Cultural , Child , Child Care , Child, Preschool , Female , Household Work , Humans , Infant , Male , Middle Aged , Philippines , Sex Factors , Time Factors , Young Adult
11.
Anim Behav ; 143: 9-24, 2018 Sep.
Article in English | MEDLINE | ID: mdl-30245525

ABSTRACT

The specialization of individuals in specific behavioural tasks is often attributed either to irreversible differences in development, which generate functionally divergent cooperative phenotypes, or to age-related changes in the relative frequency with which individuals perform different cooperative activities; both of which are common in many insect caste systems. However, contrasts in cooperative behaviour can take other forms and, to date, few studies of cooperative behaviour in vertebrates have explored the effects of age, adult phenotype and early development on individual differences in cooperative behaviour in sufficient detail to discriminate between these alternatives. Here, we used multinomial models to quantify the extent of behavioural specialization within nonreproductive Damaraland mole-rats, Fukomys damarensis, at different ages. We showed that, although there were large differences between individuals in their contribution to cooperative activities, there was no evidence of individual specialization in cooperative activities that resembled the differences found in insect societies with distinct castes where individual contributions to different activities are negatively related to each other. Instead, individual differences in helping behaviour appeared to be the result of age-related changes in the extent to which individuals committed to all forms of helping. A similar pattern is observed in cooperatively breeding meerkats, Suricata suricatta, and there is no unequivocal evidence of caste differentiation in any cooperative vertebrate. The multinomial models we employed offer a powerful heuristic tool to explore task specialization and developmental divergence across social taxa and provide an analytical approach that may be useful in exploring the distribution of different forms of helping behaviour in other cooperative species.

13.
Proc Biol Sci ; 285(1880)2018 06 13.
Article in English | MEDLINE | ID: mdl-29875307

ABSTRACT

In social mole-rats, breeding females are larger and more elongated than non-breeding female helpers. This status-related morphological divergence is thought to arise from modifications of skeletal growth following the death or removal of the previous breeder and the transition of their successors from a non-breeding to a breeding role. However, it is not clear what changes in growth are involved, whether they are stimulated by the relaxation of reproductive suppression or by changes in breeding status, or whether they are associated with fecundity increases. Here, we show that, in captive Damaraland mole-rats (Fukomys damarensis), where breeding was experimentally controlled in age-matched siblings, individuals changed in size and shape through a lengthening of the lumbar vertebrae when they began breeding. This skeletal remodelling results from changes in breeding status because (i) females removed from a group setting and placed solitarily showed no increases in growth and (ii) females dispersing from natural groups that have not yet bred do not differ in size and shape from helpers in established groups. Growth patterns consequently resemble other social vertebrates where contrasts in size and shape follow the acquisition of the breeding role. Our results also suggest that the increases in female body size provide fecundity benefits. Similar forms of socially responsive growth might be more prevalent in vertebrates than is currently recognized, but the extent to which this is the case, and the implications for the structuring of mammalian dominance hierarchies, are as yet poorly understood.


Subject(s)
Body Size , Lumbar Vertebrae/anatomy & histology , Mole Rats/physiology , Reproduction , Sexual Behavior, Animal , Animals , Female , Lumbar Vertebrae/physiology , Mole Rats/anatomy & histology
14.
Biol Lett ; 12(12)2016 12.
Article in English | MEDLINE | ID: mdl-27974493

ABSTRACT

In some eusocial insect societies, adaptation to the division of labour results in multimodal size variation among workers. It has been suggested that variation in size and growth among non-breeders in naked and Damaraland mole-rats may similarly reflect functional divergence associated with different cooperative tasks. However, it is unclear whether individual growth rates are multimodally distributed (as would be expected if variation in growth is associated with specialization for different tasks) or whether variation in growth is unimodally distributed, and is related to differences in the social and physical environment (as would be predicted if there are individual differences in growth but no discrete differences in developmental pathways). Here, we show that growth trajectories of non-breeding Damaraland mole-rats vary widely, and that their distribution is unimodal, contrary to the suggestion that variation in growth is the result of differentiation into discrete castes. Though there is no evidence of discrete variation in growth, social factors appear to exert important effects on growth rates and age-specific size, which are both reduced in large social groups.


Subject(s)
Competitive Behavior , Mole Rats/growth & development , Social Behavior , Animals , Behavior, Animal/physiology , Body Weight , Female , Male , Mole Rats/physiology , Mole Rats/psychology , Sex Factors
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