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  • 1.
    Bennett, N. C.
    et al.
    Univ Pretoria, South Africa.
    Ganswindt, A.
    Univ Pretoria, South Africa.
    Ganswindt, S. B.
    Univ Pretoria, South Africa.
    Jarvis, J. U. M.
    Univ Cape Town, South Africa.
    Zöttl, Markus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Cambridge, UK.
    Faulkes, C. G.
    Queen Mary Univ London, UK.
    Evidence for contrasting roles for prolactin in eusocial naked mole-rats, Heterocephalus glaber and Damaraland mole-rats, Fukomys damarensis2018In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 14, no 5, article id 20180150Article in journal (Refereed)
    Abstract [en]

    Elevated prolactin (PRL) has been associated with the expression of social and cooperative behaviours in a number of vertebrate species, as well as suppression of reproduction. As social mole-rats exhibit both of these traits, PRL is a prime candidate in mediating their social phenotype. While naked and Damaraland mole-rats (NMRs and DMRs) have evolved eusociality independently within their family, both species exhibit an extreme skew in lifetime reproductive success, with breeding restricted to a single female and one or two males. Non-breeding NMRs of both sexes are physiologically inhibited from reproducing, while in DMRs only the non-breeding females are physiologically suppressed. Newly emerging work has implicated the dopamine system and PRL as a component in socially induced reproductive suppression and eusociality in NMR, but the DMR remains unstudied in this context. To investigate evolutionary convergence in the role of PRL in shaping African mole-rat eusociality, we determined plasma PRL concentrations in breeders and non-breeders of both sexes, comparing DMRs with NMRs. Among samples from non-breeding NMRs 80% had detectable plasma PRL concentrations. As a benchmark, these often (37%) exceeding those considered clinically hyperprolactinaemic (25 ng ml(-1)) in humans: mean +/- s.e.m.: 34.81 +/- 5.87 ngml(-1); range 0.00-330.30 ng ml(-1). Conversely, 85% of non-breeding DMR samples had undetectable values and none had concentrations above 25 ng ml(-1): 0.71 +/- 0.38 ng ml(-1); 0.00-23.87 ngml(-1). Breeders in both species had the expected variance in plasma PRL concentrations as part of normal reproductive function, with lactating queens having significantly higher values. These results suggest that while elevated PRL in non-breeders is implicated in NMR eusociality, this may not be the case in DMRs, and suggests a lack of evolutionary convergence in the proximate control of the social phenotype in these mole-rats.

  • 2.
    Finn, K. T.
    et al.
    Rhodes Univ, South Africa;Kalahari Res Ctr, South Africa.
    Parker, D. M.
    Rhodes Univ, South Africa;Univ Mpumalanga, South Africa.
    Bennett, N. C.
    Univ Pretoria, South Africa.
    Zöttl, Markus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Kalahari Res Ctr, South Africa;Univ Cambridge, UK.
    Contrasts in body size and growth suggest that high population density results in faster pace of life in Damaraland mole-rats (Fukomys damarensis)2018In: Canadian Journal of Zoology, ISSN 0008-4301, E-ISSN 1480-3283, Vol. 96, no 8, p. 920-927Article in journal (Refereed)
    Abstract [en]

    We studied the correlates of population density and body size, growth rates, litter size, and group size in Damaraland mole-rats (Fukomys damarensis (Ogilby, 1838)) at two study sites with contrasting population densities. Group size, litter size, and the probability of recapture were independent of study site. However, body size differed between the two study sites, suggesting that population density may affect life-history traits in social mole-rats. At the low-density site (0.13 groups/ha), individuals were significantly larger and subordinate males showed higher growth rates than at the high-density site (0.41 groups/ha), which may indicate that high population density in subterranean rodents enhances pace of life. The larger size of nonreproductive individuals at the low-density site could adapt individuals at lower population densities to larger dispersal distances.

  • 3.
    Jungwirth, Arne
    et al.
    Univ Bern, Switzerland;Univ Cambridge, UK.
    Balzarini, Valentina
    Univ Bern, Switzerland;Univ Exeter, UK.
    Zöttl, Markus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Bern, Switzerland.
    Salzmann, Andrea
    Univ Bern, Switzerland;Univ Cambridge, UK.
    Taborsky, Michael
    Univ Bern, Switzerland.
    Frommen, Joachim G.
    Univ Bern, Switzerland.
    Long-term individual marking of small freshwater fish: the utility of Visual Implant Elastomer tags2019In: Behavioral Ecology and Sociobiology, ISSN 0340-5443, E-ISSN 1432-0762, Vol. 73, no 4, p. 1-11, article id 49Article in journal (Refereed)
    Abstract [en]

    Tracking wild animals over long periods of time is a non-trivial challenge. This has caused a bias in the availability of individual-based long-term datasets with the majority including birds and mammals. Visual Implant Elastomer (VIE) tags are now a widely used technique that may facilitate the collection of such data for fish and amphibians. However, VIE tags might have important drawbacks. Overall, four potential issues with VIE tags have been proposed: tag loss or misidentification, limited number of individual identifiers, enhanced mortality risk, and effects on intra-specific interactions. Here, we present three experiments in which we investigated these potential problems with VIE tagging in small freshwater fish both in the laboratory and in the wild, using the cooperatively breeding Lake Tanganyika cichlid Neolamprologus pulcher. We find VIE tags to be generally suitable for work with these fish as they did not impair survival, were recognisable up to 2years after injection, and did not generally disturb group formation. Nevertheless, we identify specific issues of VIE tagging, including colour- and position-dependent variation in tag identification rates, and indications that specific colours may influence social behaviour. Our results demonstrate the suitability of VIE tags for long-term studies on small freshwater fish, while also highlighting the need of validating this method carefully for any species and study.Significance statementInformation on the survival, dispersal, and reproductive success of wild individuals across their lifespan is among the most valuable data in Behavioural Ecology. Because tracking of free-ranging individuals over extended periods of time is challenging, there exists a bias in the taxonomic distribution of such long-term datasets. Here, we investigate the suitability of visible implant elastomers (VIE) as a tracking technique to allow for the collection of such data also in small tropical freshwater fish. We show that VIE tags neither alter social behaviour in our study species, nor do they reduce survival, but they enable the tracking of wild individuals across years. We also identify colours and tag positions that are less suitable. We conclude that VIE tags can help produce long-term datasets also for small fish, provided certain precautions are met.

  • 4.
    Thorley, Jack
    et al.
    Univ Cambridge, UK;Kalahari Res Ctr, South Africa.
    Katlein, Nathan
    Kalahari Res Ctr, South Africa;Univ S Alabama, USA.
    Goddard, Katy
    Kalahari Res Ctr, South Africa;Univ Lincoln, UK.
    Zöttl, Markus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Cambridge, UK;Kalahari Res Ctr, South Africa.
    Clutton-Brock, Tim
    Univ Cambridge, UK;Kalahari Res Ctr, South Africa;Univ Pretoria, South Africa.
    Reproduction triggers adaptive increases in body size in female mole-rats2018In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 285, no 1880, article id 20180897Article in journal (Refereed)
    Abstract [en]

    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.

  • 5.
    Thorley, Jack
    et al.
    Univ Cambridge, UK.;Kuruman River Reserve, South Africa.
    Mendonca, Rute
    Kuruman River Reserve, South Africa;Univ Neuchatel, Switzerland.
    Vullioud, Philippe
    Univ Cambridge, UK;Kuruman River Reserve, South Africa.
    Torrents-Tico, Miquel
    Kuruman River Reserve, South Africa.
    Zöttl, Markus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Cambridge, UK;Kuruman River Reserve, South Africa.
    Gaynor, David
    Kuruman River Reserve, South Africa;Univ Pretoria, South Africa.
    Clutton-Brock, Tim
    Univ Cambridge, UK;Kuruman River Reserve, South Africa;Univ Pretoria, South Africa.
    No task specialization among helpers in Damaraland mole-rats2018In: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 143, p. 9-24Article in journal (Refereed)
    Abstract [en]

    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 agerelated 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. (C) 2018 The Authors. Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

  • 6.
    Torrents-Tico, M.
    et al.
    Univ Helsinki, Finland;Univ Cambridge, UK.
    Bennett, N. C.
    Univ Pretoria, South Africa.
    Jarvis, J. U. M.
    Univ Cape Town, South Africa.
    Zöttl, Markus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Cambridge, UK.
    Sex differences in timing and context of dispersal in Damaraland mole-rats (Fukomys damarensis)2018In: Journal of Zoology, ISSN 0952-8369, E-ISSN 1469-7998, Vol. 306, no 4, p. 252-257Article in journal (Refereed)
    Abstract [en]

    Dispersal behaviour in cooperatively breeding mammals often differs between the sexes, which can affect how individuals of both sexes compete for breeding opportunities. However, it is largely unknown how the males and females in social mole-rats differ in frequency, timing and social context of dispersal. Here we show, in Damaraland mole-rats (Fukomys damarensis), that rainfall increases dispersal probabilities in both sexes. Dispersal is male biased with males dispersing earlier and more frequently in dispersal coalitions than females. Most non-reproductive individuals disperse from the natal groups before reproducing. Territory inheritance is rare, but when it occurs, female non-breeders inherit the breeding position from the precious breeding female. After dispersing from the natal group, males are more likely than females to join other established groups and to replace the resident breeder. Our study suggests that differences in dispersal strategy may generate contrasts in intra-sexual competition, where male breeders are more often challenged by competitors from outside the group and female breeders may face higher competition from individuals within the group.

  • 7.
    Torrents-Tico, Miguel
    et al.
    Univ Cambridge, UK.
    Bennett, Nigel C.
    Univ Pretoria, South Africa.
    Jarvis, Jennifer U. M.
    Univ Cape Town, South Africa.
    Zöttl, Markus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Cambridge, UK.
    Growth affects dispersal success in social mole-rats, but not the duration of philopatry2018In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 14, no 2, article id 20180005Article in journal (Refereed)
    Abstract [en]

    In naked mole-rats (Heterocephalus glaber), some non-breeding males show faster growth and are more likely to disperse than others. These differences have been suggested to be the result of a specialized developmental strategy leading to shorter philopatry and independent breeding, as opposed to extended philopatry as non-reproductive helpers. However, it is unclear whether fast-growing males disperse sooner than slow-growing males. An alternative explanation is that variation in quality between individuals causes high-quality individuals to grow quickly and maximize dispersal success without reducing philopatry. Here we show that in Damaraland mole-rats (Fukomys damarensis), males that subsequently disperse successfully grow faster than other non-reproductive males. This pattern is predicted by both hypotheses and does not discriminate between them. However, contrary to the suggestion that faster growth represents a developmental specialization for early dispersal, fast-growing and slow-growing males remained equally long in their natal groups. Our study provides no evidence for adaptive divergence in male development leading either to early dispersal or extended philopatry. Instead of representing specialized dispersers, fast-growing males of this species may be high-quality individuals.

  • 8.
    Zöttl, Markus
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Cambridge, UK.
    Vullioud, Philippe
    Univ Cambridge, UK.
    Goddard, Katy
    Kuruman River Reserve, South Africa.
    Torrents-Tico, Miquel
    Kuruman River Reserve, South Africa;Univ Helsinki, Finland.
    Gaynor, David
    Univ Pretoria, South Africa.
    Bennett, Nigel C.
    Univ Pretoria, South Africa.
    Clutton-Brock, Tim
    Univ Cambridge, UK;Univ Pretoria, South Africa.
    Allo-parental care in Damaraland mole-rats is female biased and age dependent, though independent of testosterone levels2018In: Physiology and Behavior, ISSN 0031-9384, E-ISSN 1873-507X, Vol. 193, p. 149-153Article in journal (Refereed)
    Abstract [en]

    In Damaraland mole-rats (Fukomys damal-ensis), non-breeding subordinates contribute to the care of offspring born to the breeding pair in their group by carrying and retrieving young to the nest. In social mole-rats and some cooperative breeders, dominant females show unusually high testosterone levels and it has been suggested that high testosterone levels may increase reproductive and aggressive behavior and reduce investment in allo-parental and parental care, generating age and state-dependent variation in behavior. Here we show that, in Damaraland mole-rats, allo-parental care in males and females is unaffected by experimental increases in testosterone levels. Pup carrying decreases with age of the non-breeding helper while the change in social status from non-breeder to breeder has contrasting effects in the two sexes. Female breeders were more likely than female non-breeders to carry pups but male breeders were less likely to carry pups than male non-breeders, increasing the sex bias in parental care compared to allo-parental care. Our results indicate that testosterone is unlikely to be an important regulator of allo-parental care in mole-rats.

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