Epidemiological consequences of reproductive senescence in a long-lived vector

Lead Research Organisation: Liverpool School of Tropical Medicine
Department Name: Vector Biology


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Technical Summary

Epidemiological and demographic models are essential for predicting and mitigating risks of vector-borne diseases to livestock and humans, including animal African trypanosomiasis (AAT), which is transmitted by tsetse flies. We hypothesize that failure to consider maternal investment and reproductive senescence in tsetse has limited the accuracy of models for animal trypanosomiasis.

Our aim is to improve models of tsetse population and disease dynamics, through the following objectives:
1. Establish how maternal investment changes as female tsetse age;
2. Measure the effects of maternal investment on offspring lifespan and capacity to transmit disease;
3. Elucidate how maternal effects influence tsetse population and disease dynamics.

We will achieve these objectives by combining empirical observations with evolutionary and epidemiological models. First, we will measure fat transferred by mothers to offspring, using laboratory flies of known ages and age-estimated wild flies from Zimbabwe. We will experimentally manipulate female nutrition and costs of reproduction in laboratory flies to establish the physiological determinants of age-dependent patterns. We will develop evolutionary models to ascertain whether maternal investment reflects adaptive decisions or physiological constraints.

Second, we will monitor offspring born to mothers of varying nutrition and age to establish how maternal effects influence offspring size, lifespan and reproductive success. We will infect offspring with trypanosomes to measure how maternal investment influences offspring competence at spreading disease.

Lastly, we will incorporate empirical findings into models of tsetse population and disease dynamics, using differential equation models and agent-based simulations. These models will be validated using data on tsetse abundance, host densities and trypanosome prevalence, to predict the spread of tsetse-borne disease as new habitats become suitable for this vector.

Planned Impact

Livestock keepers and communities in tsetse-suitable areas. This project will improve efforts against animal African trypanosomiasis (AAT). Some 10 million km2 of sub-Saharan Africa, covering 37 countries, are infested with tsetse and effective control of AAT could benefit people within this area. There is currently no vaccine for AAT and the only means of mitigating the disease are through tsetse control and use of trypanocides. Reducing the incidence of AAT through vector control improves cattle productivity and, ultimately, reduces poverty; currently, the loss of livestock to AAT causes annual economic losses of $4 billion. Healthier herds will improve the functioning of livestock as stores of value and indicators of social status contributing to the natural, financial and social capital of affected communities.

Policymakers in tsetse control. The project has close links to the Tsetse Control Division in Zimbabwe and outputs from our project will inform their monitoring and control efforts directly. Thus, if our project shows that maternal nutritional stress increases tsetse offspring's susceptibility to disease, our models will highlight the need for increased surveillance and trapping in areas affected by drought for several months after conditions improve, to account for carryover effects across generations. Several members of the team (Torr, Hargrove, Vale, Keeling) have strong links to national, regional and international organisations (e.g. WHO, FAO), private companies (e.g. Vestergaard, CEVA) and donors (BMGF) concerned directly with developing, supporting and implementing interventions against human and animal trypanosomiases. Outputs from this project will contribute to the knowledge that underpins the policy and practice of trypanosomiasis control being developed by these organisations.

General public. Our project is not just about predicting tsetse-borne disease, but, more broadly, understanding the profound effects that mothers can have on their offspring. This will capture the interest of the general public, as it is not generally known that tsetse - like mammals - ovulate, can get pregnant and also lactate, and thus serve as an evolutionary model of pregnancy. As an example, our project will produce evolutionary explanations for why - in a system such as mammals and tsetse, where mothers invest enormously in each offspring - mothers terminate in utero development when they are nutritionally stressed. The enormous difference between tsetse and humans notwithstanding, these few but remarkable points of similarity mean that results of our project will be of interest to our society in which maternal under- and over-nutrition is of concern, and where women are waiting until much later in life to start reproducing.


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English S (2020) The evolution of sensitive periods in development: insights from insects in Current Opinion in Behavioral Sciences

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Haines LR (2020) Big Baby, Little Mother: Tsetse Flies Are Exceptions to the Juvenile Small Size Principle. in BioEssays : news and reviews in molecular, cellular and developmental biology

Description Our project had three objectives.

First, we aimed to establish how maternal investment changes as tsetse age. To achieve this, we conducted a major laboratory-based study to test whether intraspecific variation in senescence patterns can be driven by resource availability or reproductive history. We did this by developing a novel system which allowed us to track the effects of variations in (i) nutritional stress and (ii) age at first reproduction on the age-dependent reproductive output of individual female tsetse. We found that for all treatments, offspring weight followed a bell-shaped curve with maternal age. Nutritionally-stressed females had a higher probability of abortion and produced offspring with lower starvation tolerance. There was no evidence of an increased rate of reproductive senescence in nutritionally stressed females, or a reduced rate due to delayed mating, as measured by patterns of abortion, offspring weight or offspring starvation tolerance. Therefore, although we found evidence of reproductive senescence in tsetse, our results did not indicate that resource allocation trade-offs or costs of reproduction increase the rate of senescence. These findings are reported in an article published in Ecology Letters (doi.org/10.1111/ele.13839).

We also conducted field studies in Zimbabwe where we determined the age, reproductive status and nutritional condition of tsetse caught in artificial warthog burrows. For wild-caught tsetse, we were unable to detect any effects of maternal age on offspring quality. The contrast between our laboratory- and field-based studies may be related to the fact that tsetse in the laboratory are free of the stresses associated with temperature variations and food availability that can reduce longevity in the field. Hence, those elderly females which produce poor quality offspring in the laboratory might never reach old age in the field. .

Our second objective was to measure the effects of maternal investment on offspring lifespan and capacity to transmit disease. For the latter, we conducted laboratory studies in which we infected offspring with trypanosomes to measure how maternal investment influences offspring competence at spreading disease. Analyses of ~1200 tsetse showed that there was no significant effect of maternal age on the vector competence of their offspring.

Our third objective was to elucidate how maternal effects influence tsetse population and disease dynamics. To achieve this, we aimed to incorporate empirical findings into models of tsetse population and disease dynamic. Since we found strong evidence for the effects of environmental temperature but not maternal effects, our models focussed on the effects of the former. Highlights from our modelling work include a study (doi.org/10.1371/journal.pmed.1002675) showing that climate-related increases in temperature may explain the decline in tsetse abundance in the Zambezi Valley of Zimbabwe. Building on this model, we also examined how increases in temperature may have changed the distribution and abundance of tsetse across northern Zimbabwe (doi.org/10.1186/s13071-020-04398-3). The model predicts that temperature changes in the period 2000-2016 have decreased the abundance of tsetse in low elevation areas but increased it in high ones (> 1000 m above sea level); areas previously considered too cold to sustain tsetse, may now be climatically suitable.

Finally, we also produced evolutionary models to analyse the trade-off between allocating current resources to reproduction versus maximizing survival to produce further offspring. For many taxa, including tsetse, parental allocation varies across age following a hump-shaped pattern. This nonlinear allocation pattern lacks a general theoretical explanation. We developed a life-history model of maternal allocation in tsetse to identify the optimal allocation strategy in response to stochasticity when energetic costs, feeding success, energy intake and environmentally driven mortality risk are age-dependent. Diverse scenarios generate a hump-shaped allocation when energetic costs and energy intake increase with age and also when energy intake decreases and energetic costs increase or decrease. We suggest that age-dependence in these traits explain the prevalence of nonlinear maternal allocation across diverse taxonomic groups (doi.org/10.1098/rspb.2021.1884).
Exploitation Route Data from our studies will contribute to epidemiological models of trypanosomiasis which will guide the policy and practice of programmes to control human and animal trypanosomiasis.
Sectors Agriculture, Food and Drink,Healthcare

Title Novel method for analysing the larviposition behaviour of tsetse flies 
Description We developed a lab-based assay which allows us to record the production of larvae by tsetse. 
Type Of Material Technology assay or reagent 
Year Produced 2017 
Provided To Others? No  
Impact None to date but a publication reporting the method is expected in 2020. 
Title Model of the impact of climate change on tsetse populations 
Description An ODE model which analyses the impact of changes in environmental temperature on the dynamics of tsetse populations. 
Type Of Material Computer model/algorithm 
Year Produced 2018 
Provided To Others? Yes  
Impact No notable impact to date. 
URL https://journals.plos.org/plosmedicine/article?id=10.1371/journal.pmed.1002675
Description Bristol 
Organisation University of Bristol
Country United Kingdom 
Sector Academic/University 
PI Contribution Expertise in tsetse biology
Collaborator Contribution Expertise in evolutionary theory and modelling
Impact None produced to date but we expect publications in 2020
Start Year 2016
Description SACEMA 
Organisation University of Stellenbosch
Country South Africa 
Sector Academic/University 
PI Contribution Field- and laboratory-based investigations of tsetse.
Collaborator Contribution Development of models of tsetse populations.
Impact Joint publications (see Publications Outputs)
Start Year 2014
Description ENVT summer school 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Lecture on tsetse biology and control to a summer school comprising post-graduate students and early-career researchers from Europe and Africa. The summer school is organised and hosted by the École Nationale Vétérinaire de Toulouse
Year(s) Of Engagement Activity 2019
URL http://www.envt.fr/content/universit%C3%A9-d%E2%80%99%C3%A9t%C3%A9-en-entomologie-m%C3%A9dicale-et-v...
Description Panelist (1/4) for an on-line discussion about elimination of HAT 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact An international meeting convened by the London Centre for Neglected Tropical Diseases and the HAT platform. The 3-day programme was concerned about research priorities to support the achievement of WHO's goal goal of eliminating transmission of HAT by 2030. Prior to the meeting, presentations were produced on a range of relevant topics. These included a presentation on tsetse control produced by Drs Inaki Tirados and Andrew Hope from LSTM. I was an invited panelist for a 2 hour live on-line discussion concerned with vector control and diagnostics.
Year(s) Of Engagement Activity 2022
URL https://www.londonntd.org/news/lcntdr-the-hat-platform-scientific-research-meeting-achieving-human-a...
Description Short film on the project presented at Bristol Science Festival, 2021 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact The short film, entitled "Burrowing For Knowledge" is a mini-documentary which describes an international project to understand the reproductive ecology of tsetse. T
Year(s) Of Engagement Activity 2021
URL https://www.youtube.com/watch?v=2-dekOKCoRA
Description TsetseNet Ghana 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presentation by Dr Jennifer Lord on "Tsetse and animal African trypanosomiasis control amid rapid anthropogenic change"
Year(s) Of Engagement Activity 2020