Genetic traces of hierarchy: How social standing shapes the epigenome of Tanzania’s Spotted Hyenas
Spotted hyenas (Crocuta crocuta) resting at the communal den in the Serengeti National Park in Tanzania. (Picture: S. Benhaiem)
The researchers analysed DNA from three clans of spotted hyenas (Crocuta crocuta) in the Serengeti National Park, Tanzania. (Picture: Wikimedia Commons - Tubs)
Spotted hyenas (Crocuta crocuta) are highly social animals with a predictable social status determined by family relationships and behavioural conventions. (Picture: Wikimedia Commons - A. Peach)
New study reveals how social status and behaviour are reflected in the genetic makeup
Based on a media release from the Leibniz Institute for Zoo and Wildlife Research (Leibniz-IZW)
A research consortium led by scientists from the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig and the Leibniz Institute for Zoo and Wildlife Research (Leibniz-IZW) provide evidence that social behaviour and social status are reflected at the molecular level of gene activation (epigenome) in juvenile and adult free-ranging spotted hyenas. The results, published in the scientific journal Communications Biology, contribute to a better understanding of the role of epigenetic mechanisms in the interplay of social, environmental and physiological factors in the life of a highly social mammal.
In mammals, social behaviour and social status can substantially influence the survival, reproductive performance and health of individuals. However, it is not yet fully understood how the translation of social and environmental factors into the physiology of an organism is reflected in molecular processes. Now, scientists have found that social status influences epigenetic patterns, more specifically, the methylation of DNA in both young and adult female spotted hyenas (Crocuta crocuta), which determines the activation of genes. They analysed DNA from gut epithelium cells from 18 adult female hyenas and 24 cubs with known social status from three clans in the Serengeti National Park, Tanzania. The scientists identified and validated 149 genome regions where high-ranking and low-ranking individuals differed in the methylation of DNA (differentially methylated regions, DMRs). “We could, for the first time, provide evidence for epigenetic signatures of social inequalities in both young and adult spotted hyenas”, says senior author Dr Alexandra Weyrich, sDiv scientist at iDiv and head of the working group “Wildlife Epigenetics” at the Leibniz-IZW. “We hope that in the future epigenetic biomarkers can be incorporated in biodiversity research to understand species‘ responses to environmental differences better”.
The findings show that these epigenetic signatures are stable across life stages – and that they are linked to important physiological processes: Many of the identified DMRs were involved in the regulation of energy conversion, immune response, glutamate receptor signalling and ion transportation. “Especially the large number of DMRs in genes involved in energy conversion caught our eye”, says first author Colin Vullioud, data scientist in Weyrich’s working group. Co-author Dr Sarah Benhaiem, co-head of the Serengeti Hyena Project, explains: “We suspect that this may be driven by differences in behaviour and specifically the greater use of long-distance foraging trips by low-ranking than high-ranking females – the latter monopolising resources in their clan territory.” Interestingly, these genes were more methylated (or hypermethylated) in low-ranking adult females but not in cubs. This could indicate an adjustment of low-ranking adult females to higher energetic costs of frequent long-distance commuting, a behaviour not displayed by cubs. “Although the exact physiological consequences of the observed hypermethylation remain to be investigated, these findings are consistent with our observations and hint at the sought-after missing link between social and physiological factors”, according to Weyrich and Benhaiem.
The analyses build on long-term research on spotted hyenas in the Serengeti, which started in 1987. The females in this investigation are individually known, and their social status has been tracked for generations. This provided ideal conditions to study the links between behaviour, physiological factors, epigenetic modifications and fitness in terms of survival and reproduction in a wild population. The use of faecal samples collected in a non-invasive manner is one of the strengths of the investigation, the authors surmise. “The capture methylation method we used enriches methylated DNA as well as mammalian DNA, which improved the amount of hyena DNA over bacterial DNA and the quality of the sequencing data”, Weyrich explains.
DNA methylation is a chemical modification of the basic building blocks of a cell's genetic material. This modification is enabled by the transfer of methyl groups to nucleobases at certain positions in the DNA. As the basic structure of the respective nucleobase is unaltered, DNA methylation is not a genetic mutation but a modification which determines whether this part of the DNA is ‘being used’ (activated) or switched off. DNA methylation is the most important epigenetic modification and, thus, a pivotal part of making genetic information available to the physiological processes within a cell.
Spotted hyenas are highly social animals and an excellent example of how differences in physiological processes and health can accompany status-related differences. In hyena clans, females and their offspring socially dominate all immigrant males, and social status is behaviourally “inherited” by cubs from mothers who gain privileges associated with maternal social status. Therefore, social status is stable and predictable because it is determined by family relationships and behavioural conventions.
“Additionally, the effects of social status on life history trajectories and health are typically passed across generations”, adds Heribert Hofer, Director of Leibniz-IZW. For example, high-ranking females have priority access to resources in the clan territory and do not need to commute as much as low-ranking females to find food. They are, therefore, much more often present at the communal den and nurse their young more frequently. The milk-dependent cubs disproportionally benefit at this early stage in their life – by growing faster, having a higher chance of surviving to adulthood and starting reproduction at an earlier age than the offspring of low-ranking females.
Original Publication
Vullioud C, Benhaiem S, Meneghini D, Szyf M, Shao Y, Hofer H, East ML, Fickel J, Weyrich A (2024): Epigenetic signatures of social status in female free-ranging spotted hyenas (Crocuta Crocuta). Communications Biology.DOI: 10.1038/s42003-024-05926-y
Contact:
Dr Alexandra Weyrich(English, German)
Postdoctoral Researcher
sDiv - Synthesis Centre
German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig
Phone: +49 341 9733224
Email: alexandra.weyrich@idiv.de
Kati Kietzmann
Media and Communications
German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig
Phone: +49 341 9739222
Email: kati.kietzmann@idiv.de
