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Social below ground: Life-history and gut microbiome of Damaraland mole-rats
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.ORCID iD: 0000-0002-8449-9843
2023 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Studying the consequences of variation in individual life-histories is vital for our understanding of the evolution of animal societies. In this thesis, I study the ecology and consequences of group living on growth, survival, reproduction, and the gut microbiome of the Damaraland mole-rat (Fukomys damarensis), a subterranean cooperatively breeding mammal. For this, I used data and faecal samples collected from a long-term study population in the Kalahari Desert, South Africa.

I explored the effects of group size and group composition on individuals’ growth and survival. While large group size had no clear advantages for either growth or survival, individuals within groups biased to their own sex grew more slowly. The number of recruits increased modestly with group size, but experimentally created pairs showed the same reproductive success as established groups. Further, single individuals exhibited high survival rates and good body condition. Combined, these results suggest that mole-rats delay dispersal to maximise their own fitness, and that group living has costs and benefits for all group members.

I also investigated the effects of individual life-histories and group affiliation on the gut microbiome. This work shows that individuals bring the gut microbiome from their birth group when they disperse, and that group members have more similar gut microbiomes. When dispersed individuals start to reproduce in their new groups, they subsequently transfer this microbiome to their offspring, resulting in higher similarity between offspring with common descent of breeders. This pattern could arise from shared early life environment of breeders or through genetic relatedness of breeders. To separate the effects of these factors, I used a cross-foster experiment of captive animals, which showed that group members have more similar gut microbiomes, regardless of host relatedness.

My thesis gives deepened insights into the ecology of the Damaraland mole-rat. It shows how variation in the social environment of group living species affects their life-histories, their fitness, and beyond that extended phenotypic traits such as the gut microbiome composition.

Place, publisher, year, edition, pages
Linnaeus University Press, 2023. , p. 61
Series
Linnaeus University Dissertations ; 512
National Category
Ecology Evolutionary Biology
Research subject
Ecology, Evolutionary Biology; Natural Science, Ecology
Identifiers
URN: urn:nbn:se:lnu:diva-125469DOI: 10.15626/LUD.512.2023ISBN: 9789180821001 (print)ISBN: 9789180821018 (electronic)OAI: oai:DiVA.org:lnu-125469DiVA, id: diva2:1809436
Public defence
2023-12-08, Sal Fullriggaren, Hus Magna, Kalmar, 09:00 (English)
Opponent
Supervisors
Available from: 2023-11-07 Created: 2023-11-03 Last updated: 2023-11-17Bibliographically approved
List of papers
1. Damaraland mole-rats do not rely on helpers for reproduction or survival
Open this publication in new window or tab >>Damaraland mole-rats do not rely on helpers for reproduction or survival
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2023 (English)In: Evolution Letters, E-ISSN 2056-3744, Vol. 7, no 4, p. 203-215Article in journal (Refereed) Published
Abstract [en]

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. Lay Summary Social mole-rats are subterranean rodents that live in family groups where a single breeding female is responsible for the production of all pups. It has frequently been suggested that her non-breeding offspring act as helpers and increase the survival of all group members through cooperative foraging, which is thought to increase the rate at which tubers and other geophytes-the principal food of mole-rats-are found. Such helper effects are expected to generate positive associations between group size and reproduction, growth, and survival, but have rarely been looked for in wild populations. After monitoring a population of Damaraland mole-rats in the Southern Kalahari over 7 years, we found that the effect of non-breeders on the reproductive output of breeding females was modest: large groups recruited only slightly more offspring than smaller groups, and the experimental creation of breeding pairs showed that newly formed groups can start breeding immediately and reproduce at rates comparable to established groups. Effects of group size on individual growth rates and on individual survival were also limited, with solitary females in particular-females who have dispersed from their natal group and settled alone-showing high survival rates that approached that of breeding females. Taken together, our results suggests that the extent to which breeding females rely on non-breeders as helpers in mole-rat societies may be less pronounced than previously thought. Helper effects appear relatively weak and the principal reason that offspring delay dispersal is likely because of the strong constraints on dispersal in this species.

Place, publisher, year, edition, pages
Oxford University Press, 2023
Keywords
sociality, cooperative breeding, helper effects, philopatry, family living
National Category
Evolutionary Biology Ecology
Research subject
Ecology, Evolutionary Biology; Natural Science, Ecology
Identifiers
urn:nbn:se:lnu:diva-122879 (URN)10.1093/evlett/qrad023 (DOI)000996756500001 ()
Available from: 2023-06-28 Created: 2023-06-28 Last updated: 2023-11-03Bibliographically approved
2. Within-group sex ratios predict growth of social mole-rats
Open this publication in new window or tab >>Within-group sex ratios predict growth of social mole-rats
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Groups of wild animals can vary considerably in their composition, including in the proportion of group members which are male or female, the within-group sex ratio. Variation in within-group sex ratios can arise from active adjustment of litter sex ratios by mothers, from sex differences in mortality, dispersal and immigration, or from stochastic variation in recruitment. Irrespective of its origins, variation in the within-group sex ratio can have consequences for within-group competition and can affect individual life histories throughout development. In this paper, we explore which processes may generate variation in within-group sex ratios in wild Damaraland mole-rats (Fukomys damarensis), a singular cooperative breeder, and we investigate whether within-group sex ratios predict the growth, body condition and philopatry of individuals. We show that although the population-level sex ratio is balanced, skewed within-group sex ratios are common, particularly among small groups. Our data suggests that stochastic variation in the sex of recruits explains natural variation in the sex ratio of wild groups. Non-breeding individuals in groups with a sex ratio biased towards their own sex grow more slowly than individuals in groups biased towards the opposite sex, suggesting that intra-sexual competition may decrease growth rates. We suggest that the costs of competition may contribute to the large variation in growth observed in social mole-rat groups.

Keywords
sex ratio, growth, intra-sexual competition, cooperative breeding, Damaraland mole-rat
National Category
Ecology Zoology Evolutionary Biology
Research subject
Ecology, Evolutionary Biology
Identifiers
urn:nbn:se:lnu:diva-125460 (URN)
Available from: 2023-11-03 Created: 2023-11-03 Last updated: 2023-11-07Bibliographically approved
3. Gut microbiome similarity in wild mole-rats: The effects of shared common descent
Open this publication in new window or tab >>Gut microbiome similarity in wild mole-rats: The effects of shared common descent
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Group members often show high similarity in their gut microbiomes. This is typically attributed to increased social transmission of microbes within social groups and the shared environment. However, despite extensive research on within-group variation in gut microbiomes of wild hosts, between-group variation has remained less explored. Here, we use faecal samples collected from a long-term study population of wild Damaraland mole-rats (Fukomys damarensis) to study within- and between group variation in gut microbiome similarity. We show that overall, group members have more similar gut microbiomes than those of individuals from separate groups. For individuals who had dispersed to become breeders in separate groups, dispersal from the same birth group predicted more similar microbiomes. The birth group affiliation therefore has long lasting effects on the microbiome, which individuals bring with them as they disperse to establish their own groups. Our results also suggest that when these individuals start to breed, their gut microbiome is transferred to their offspring, who show higher microbiome similarity if their parents shared birth groups. Together, we show that the gut microbiome can be transferred over generations and variation between groups can be predicted by the dispersal histories of individuals. Although we also identify some environmental effects on the gut microbiome within the population, our study shows that the gut microbiome can be inherited through shared common descent of the parental generation. Our results help to explain similarities in gut microbiomes within and between groups of social mammals.

Keywords
Gut microbiome, 16S rRNA gene amplicon, social, mammal, life-history, transgenerational effects, Damaraland mole-rat, group living, microbiome similarity
National Category
Evolutionary Biology Ecology Microbiology
Research subject
Ecology, Evolutionary Biology
Identifiers
urn:nbn:se:lnu:diva-125465 (URN)
Available from: 2023-11-03 Created: 2023-11-03 Last updated: 2023-11-07Bibliographically approved
4. Environmental effects rather than relatedness determine gut microbiome similarity in a social mammal
Open this publication in new window or tab >>Environmental effects rather than relatedness determine gut microbiome similarity in a social mammal
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2023 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 36, no 12, p. 1753-1760Article in journal (Refereed) Published
Abstract [en]

In social species, group members commonly show substantial similarity in gut microbiome composition. Such similarities have been hypothesized to arise either by shared environmental effects or by host relatedness. However, disentangling these factors is difficult, because group members are often related, and social groups typically share similar environmental conditions. In this study, we conducted a cross-foster experiment under controlled laboratory conditions in group-living Damaraland mole-rats (Fukomys damarensis) and used 16S amplicon sequencing to disentangle the effects of the environment and relatedness on gut microbiome similarity and diversity. Our results show that a shared environment is the main factor explaining gut microbiome similarity, overshadowing any effect of host relatedness. Together with studies in wild animal populations, our results suggest that among conspecifics environmental factors are more powerful drivers of gut microbiome composition similarity than host genetics.

Place, publisher, year, edition, pages
John Wiley & Sons, 2023
Keywords
16S, environmental effects, group living, gut microbiome, relatedness
National Category
Ecology
Research subject
Natural Science, Ecology
Identifiers
urn:nbn:se:lnu:diva-124071 (URN)10.1111/jeb.14208 (DOI)001049289200001 ()37584218 (PubMedID)2-s2.0-85168146294 (Scopus ID)
Available from: 2023-09-05 Created: 2023-09-05 Last updated: 2024-01-18Bibliographically approved
5. Freeze-drying can replace cold-chains for transport and storage of fecal microbiome samples
Open this publication in new window or tab >>Freeze-drying can replace cold-chains for transport and storage of fecal microbiome samples
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2022 (English)In: PeerJ, E-ISSN 2167-8359, Vol. 10, article id e13095Article in journal (Refereed) Published
Abstract [en]

Background: The transport and storage of samples in temperatures of minus 80 °C is commonly considered as the gold standard for microbiome studies. However, studies conducting sample collection at remote sites without a reliable cold-chain would benefit from a sample preservation method that allows transport and storage at ambient temperature.

Methods: In this study we compare alpha diversity and 16S microbiome composition of 20 fecal sample replicates from Damaraland mole-rats (Fukomys damarensis) preserved in a minus 80 °C freezer and transported on dry ice to freeze-dried samples that were stored and transported in ambient temperature until DNA extraction.

Results: We found strong correlations between relative abundances of Amplicon Sequence Variants (ASVs) between preservation treatments of the sample, no differences in alpha diversity measures between the two preservation treatments and minor effects of the preservation treatment on beta diversity measures. Our results show that freeze-drying samples can be a useful method for cost-effective transportation and storage of microbiome samples that yields quantitatively almost indistinguishable results in 16S microbiome analyses as those stored in minus 80 °C.

Place, publisher, year, edition, pages
PeerJ, 2022
Keywords
16S, Amplicon, DNA metabarcoding, Damaraland mole-rat, Fecal samples, Freeze-drying, Fukomys damarensis, Microbiome
National Category
Microbiology
Research subject
Natural Science, Ecology
Identifiers
urn:nbn:se:lnu:diva-111402 (URN)10.7717/peerj.13095 (DOI)000798603700002 ()35310158 (PubMedID)2-s2.0-85127083614 (Scopus ID)2022 (Local ID)2022 (Archive number)2022 (OAI)
Available from: 2022-04-19 Created: 2022-04-19 Last updated: 2023-11-03Bibliographically approved

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Bensch, Hanna

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