Trans-generational costs of reproduction and the evolution of life histories

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

Why do some individuals in a population deteriorate much more rapidly with age than others? This is a question of great biological and biomedical importance, but remains a puzzle. Current theory is based on the idea that reproduction is costly: individuals that invest more in current reproduction pay a cost in terms of reduced future reproductive success and survival. There is lots of evidence to support this proposed cost of reproduction, but the underlying mechanisms remain controversial. One major theory is that reproduction entails increased levels of oxidative damage, which can have negative consequences for the functioning of cells and tissues, and thereby reduce survival. However, evidence that reproduction increases oxidative damage is equivocal: in some contexts breeding individuals show higher levels of oxidative damage, but a growing number of studies show the opposite pattern.

We recently suggested that previous results can be explained if oxidative damage has negative impacts not just on mothers, but also on their developing offspring, i.e. if there are trans-generational costs of reproduction. In these circumstances mothers could gain from reducing their own levels of oxidative damage to shield their offspring from harm during sensitive developmental windows - the 'oxidative shielding' hypothesis (OSH). Trans-generational impacts of oxidative damage could have a major impact on patterns of growth, reproduction, and survival, but we currently have almost no theory to understand these impacts.

Our goal is to develop this new theory of trans-generational costs of reproduction, and to carry out the first test of the OSH and our new models in a tractable wild mammal study system, the banded mongoose. It is particularly powerful to test life history theory in natural populations, where trade-offs can be measured together with their consequences for fitness. The banded mongoose is uniquely suited to our objectives because we know the full breeding history and pedigree of all animals, and we can experimentally manipulate the nutritional condition of mothers during pregnancy and follow the development and success of their offspring as they grow up and start to breed themselves.

The project will advance conceptual understanding of why individuals vary so much in patterns of development and reproduction, and help to answer the question of why some individuals survive longer than others. Our theoretical framework could readily be applied to study other forms of damage that carry-over to affect offspring, such as heavy metal poisoning, or transmissible parasites and pathogens. The project fits squarely with NERC's strategy priorities to manage environmental change and understand the resilience of natural populations to environmental hazards, because both of these priorities require improved understanding of how individuals defend against environmental challenges and stressors, and how perturbations experienced by one generation reverberate through to influence the viability of future generations.

Planned Impact

Who will benefit from this research?
A key target group will be other academics, who will be engaged with via standard activities (publishing our research, presenting scientific seminars, attending conferences). In addition, the main non-academic beneficiaries from the proposed research will be 1) the general public, secondary teachers and their students; and 2) the Uganda Wildlife Authority, and Uganda Tourist Board.

How will they benefit from this research?
The proposed work is largely curiosity-driven, but we are contributing to understanding of an issue of great significance to most people. Understanding why some individuals deteriorate rapidly with age, whereas others live relatively long and healthy lives is an issue of concern to almost every country. There is particular public interest in the early-life origins of health and longevity. Our findings are therefore likely to be of interest to the general public, secondary education teachers and their students, both in the UK and in Uganda. Social mammals are intrinsically appealing to the public and we aim to capitalise on this interest to improve the public understanding of science. The general public, teachers and their students will directly benefit through education, international cultural exchange, and engagement with scientific research.

The project team has established relations with the Uganda Wildlife Authority and Uganda Tourist Board who will benefit through the information exchange aspects of the project. This will help to promote ecotourism and investment in Uganda's protected areas, and increase local and international awareness of its natural resources.

Finally, the project team including the PDRA will benefit from developing new skills and experience in outreach and engagement with beneficiaries of the research, which will enhance career development.

Publications

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Description In this project we have investigated the role that oxidative stress plays in shaping reproduction. In particular, we have explored the possibility that oxidative damage may constrain the level of investment in reproduction that mothers can afford to make. We have also examined the extent to which investment in reproduction may cause damaging increases in oxidative damage levels in mothers. Finally, we have investigated the associations between oxidative damage levels in pregnant mothers and the growth and survival of their pups. This part of the project has involved a test of the 'oxidative shielding' hypothesis - the idea that mothers could gain from reducing their own levels of oxidative damage to shield their offspring from harm during sensitive periods in early development, such as during pregnancy and lactation.

Our wild banded mongoose study system combines long-term monitoring of all the major events in the lives of individuals from birth to death. Unusually for a long-term field study of a wild animal, we have been able to use an experimental (food provisioning) approach to understand the role that maternal nutrition plays in shaping oxidative stress and reproduction. Banded mongooses are cooperative breeders and give birth synchronously, which allows for a powerful experiment design that includes both provisioned and non-provisioned (control) females producing offspring in the exact same environment.

We have found that oxidative stress shapes reproduction in multiple ways. Breeding poses an oxidative challenge, which appears to be mitigated by mothers both by constraining their subsequent investment in reproduction, but also by decreasing oxidative damage levels compared to non-breeders. We think such reductions serve to shield mothers and their offspring from the negative consequences of oxidative stress. Indeed, our results show that levels of oxidative stress in breeding mothers predict the long-term survival of their offspring, thus highlighting the importance of mitigating the oxidative cost of reproduction.
Exploitation Route The outcomes of this project advance understanding of how physiological stress can affect patterns of development, reproduction and survival. This will be of interest to ecologists and evolutionary biologists, and also medical and veterinary scientists interesting in understanding why individuals vary so much in how much they invest in reproduction and how long they live. Our results are also relevant to government policy in the context of environmental contamination, safeguarding and mitigation (for example the UK government's 25 year environment plan). We provide important new insights into the ways in which physiological stress can have damaging consequences that transmit across generations, and the extent to which mothers may benefit by mitigating such effects. This has applied relevance because many environmental contaminants have potential to cause oxidative stress, to bioaccumulate, and to transmit across generations. More broadly, the theoretical framework that we are developing as part of our project will enable prediction of inter-generational impacts of a range of environmental contaminants.
Sectors Other

 
Description The main non-academic impact to date is via the development of an online digital game where players must make key decisions in the lives of mongooses, such as how often to reproduce and how many resources to invest in the production of high-quality offspring. This informs understanding about the ways in which trade-offs in the allocation of the body's resources can influence health, reproduction and survival, and how a mother's own body condition can have impacts that transmit to her offspring and affect their development and survival.
First Year Of Impact 2021
Sector Education
Impact Types Societal

 
Description 60000
Amount £60,000 (GBP)
Funding ID 640002321 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 08/2019 
End 02/2023
 
Title Banded Mongoose Social Network Edge Lists and Nodes - Simulated Intergroup Conflict 
Description Social interaction edge lists and nodes for banded mongoose groups (1B, 1H, 2, 11 and 26). Two types of interaction were recorded - grooming (grooming and nubbing affiliative behaviours), and aggression (all types of aggression - over food, mates or dominance). Observations took place before or after a simulated intergroup conflict (R1-6) or control (C1-7) presentation. The conflict included presentation of faeces and scent marks from a rival group, playback of war cries and presentation of four adult male rival individuals. The control included presentation of faeces and scent marks from their own pack, playback of neutral communication calls from their own pack, and presentation of four of their own males. Nodes contain individual identity and traits including sex and age. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Banded_Mongoose_Social_Network_Edge_Lists_and_Nodes_-_Simulate...
 
Title Code, data & README for PAG et al: "Collective defence and behavioural homogeneity during simulated territorial intrusions in banded mongooses (Mungos mungo)." 
Description All data, R codes, and a README file associated with the manuscript: "Testing the conflict-cohesion hypothesis: metrics of social cohesion during simulated territorial intrusions in banded mongooses (Mungos mungo)." 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Code_data_README_for_PAG_et_al_Collective_defence_and_behaviou...
 
Title Code, data & README for PAG et al: "Collective defence and behavioural homogeneity during simulated territorial intrusions in banded mongooses (Mungos mungo)." 
Description All data, R codes, and a README file associated with the manuscript: "Testing the conflict-cohesion hypothesis: metrics of social cohesion during simulated territorial intrusions in banded mongooses (Mungos mungo)." 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Code_data_README_for_PAG_et_al_Collective_defence_and_behaviou...
 
Description Development of a digital game 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact In collaboration with internationally renowned educational game developers 'Then Try This' (www.thentrythis.org), we have developed a fun and engaging online game where players must make key decisions as the lives of individual mongooses unfold. The game is called 'Marvellous Mongooses', and is designed to explore the consequences of parental condition for reproductive performance, and how parental condition can impact on offspring. Players are asked to put themselves in the shoes of individual mongooses living in the African savannah. They start the game with a group of mongooses that they have to help prosper. To do so, they must make decisions that mongooses face in daily life, such as what food to eat, what age to start breeding, how often to breed, how many pups to produce, how much time to spend guarding offspring against predation, and how much energy to invest in each pup. Players witness the consequences of their decisions in terms of numbers of surviving offspring, health of these offspring, and changes in the size of the group. Overall, the game allows players to explore how maternal condition can have inter-generational impacts on offspring, in addition to encourage understanding from another species' perspective.
Year(s) Of Engagement Activity 2021,2022
URL https://mongoose.thentrythis.org/