Understanding causes and consequences of the extreme thermal sensitivity of male fertility using a model insect

Lead Research Organisation: University of East Anglia
Department Name: Biological Sciences

Abstract

Male fertility is a key biotic trait with exceptional sensitivity to a fundamental abiotic variable: temperature. We have long known that male mammals suffer infertility if ambient or testicular temperatures rise, and we are just recognising the same phenomenon in cold-blooded species, whose physiology is directly affected by temperature changes. In nematodes, fruitflies and flour beetles, we now know that after conditions mimicking a natural heatwave, male fertility decreases to a point where population viability is impossible solely due to male sterility. Female fertility, by contrast, is unaffected across the same temperatures.
Because (a) male fertility allows populations to persist, (b) climate extremes are increasing, and (c) most of the world's biodiversity is cold-blooded and reproduces sexually, we propose to understand how heatwave conditions impact upon reproduction. We need to know which male stages and traits are so sensitive, how quickly they recover, and whether male fertility can adapt or evolve to warmer regimes. To provide answers, we will use a model insect: the flour beetle Tribolium castaneum which (1) we can culture and experimentally replicate to high levels, (2) has detailed assays for measuring fertility, reproduction and sperm form and function, and (3) has a short generation time for experimental evolution. Importantly, we have established that T. castaneum male fertility is characteristically sensitive to thermal change: treatments on young adults that mimic 5-day heatwaves (expected to increase 10-fold this century), create male fertility declines of 20 to 50% in temperatures 2.5C to 5C above the population productivity optimum. Males become sterile 7.5C above the optimum, whereas female fertility is unaffected by these treatments.
This background means that (i) thermal change constrains T. castaneum fertility, (ii) we can run controlled experiments with high replication to determine the specific effects of temperature on male fertility, its recovery in the laboratory, and the consequences for population productivity, (iii) we can measure these effects in vitro (via sperm form and function assays) and in vivo (via offspring and population productivity) to gain mechanistic and predictive insight, and (iv) the development and generation times allow us to measure how populations acclimate and evolve to thermal change. We therefore aim to answer the following key questions to understand the individual causes, and population and evolutionary consequences, of thermosensitive male fertility:
A. When is male fertility sensitive to thermal change, what are the specific effects on sperm development, form and function, what is the capacity for recovery, and what are the population-level effects?
- Here, we will assess windows of sensitivity, by isolating thermal effects at separate developmental stages of germ cells, spermatogenesis and/or mature sperm form and function. We will measure how thermal treatment (at different developmental stages) affects sperm quantity and quality using different assays of sperm degeneration. Re-tests of male fertility after treatment will measure rate and extent of recovery, and population consequences will allow predictions for the natural environment.
B. What is the rate and extent of acclimation and adaptation of male fertility and sperm to new thermal regimes?
- We need to understand the capacity of populations to adapt male fertility to cope with more frequent thermal stress, so here we will conduct within-generation heat hardening tests and a 3-year replicated experimental evolution trial, which together will quantify the extent and rates of adaptation in the tolerance of male fertility to novel thermal regimes.
C. Can female mating pattern mitigate against male infertility?
- Here we will test whether costly female promiscuity, and sperm selection into storage, improve population productivity in the face of male subfertility because of hyperthermia.

Planned Impact

Within the natural environment, one of the most pervasive abiotic variables is temperature, and one of the most universal biotic functions is sexual reproduction. Understanding the details of the relationship between temperature and male fertility will have impacts that range from sperm biology to conservation ecology. Our project has relevance to those interested in Climate Change, and with UEA as an important hub for this research we have access to scientific end-users across a broad set of overlapping fields.

RELEVANCE TO WIDER SCIENTIFIC END-USERS
- Conservation and evolutionary ecologists. The impact of rapid temperature change on the world's biodiversity will be huge. Despite this, a recent review concluded: 'there is almost no species for which we know enough relevant ecology, physiology and genetics to predict its evolutionary response to climate change' (Gienapp et al 2008). Our project aims to address this deficit, using experimental studies in a model insect system, with impact for evolutionary and conservation biologists. Our proposal will measure how thermal stress impacts directly on male fertility, sperm form and function, and the consequences for population viability. By measuring and tracking the adaptive and evolutionary responses of a key biotic trait to a fundamental abiotic force, the work will impact on researchers in evolutionary ecology, both through implications for community ecology, and the understanding of adaptation to novel thermal regimes. We will retain DNA throughout acclimation and evolution experiments, which will be made available to projects seeking to link genomic changes (using the completed Tribolium genome sequence) with our phenotypic response results.
- Reproductive and sperm biologists. The project will enhance our functional and evolutionary understanding of sperm biology, with consequences for pure understanding of spermatogenesis and sperm form and function.
- Andrologists and animal breeders. There is pure and applied relevance to research into the importance of thermal stress for male fertility in mammalian systems, including humans.

RELEVANCE TO NON-SCIENTIFIC END-USERS
Sexual reproduction, sperm biology and climate change have intuitive appeal to the public. The project will identify (1) the importance of male infertility under thermal stress for population viability, (2) the phenotypic mechanisms responsible, and (3) the capacity of populations and lineages to adapt under thermal stress. If our results indeed reveal that thermosensitive male fertility could be a driver of population viability under climate warming, then our research will directly inform on one mechanism that could create population range shifts or local extinction under climate change, and important findings will be given maximum publicity, including online video presentations, as we produced through You Tube for our recent paper in Science.

PLANS FOR ACHIEVING IMPACT & MILESTONES: SCIENTIFIC END-USERS
Because our aims have broad impact, we plan to publish the primary research findings in rapid turn-around, international-impact journals. We will deliver talks at international conferences focusing on the overlapping fields of evolutionary biology, conservation biology, and sperm biology. We will organise and host a 2-day workshop at UEA on 'Climate Warming and Adaptation', to which we will also invite policy-makers.

PLANS FOR ACHIEVING IMPACT & MILESTONES: NON-SCIENTIFIC END-USERS
In conjunction with our press office, we will achieve targeted publicity of all outputs via advanced press releases, and communicate our work within UEA. All of the research team will engage with the various media outlets to achieve maximum and accurate communication. We will produce and maintain an active project website, to include a 'beetlecam' live magnified video feed of flour beetle activities. We will participate in the Royal Society Summer Science Exhibition, as discoveries of exciting impact are made.
 
Description Male fertility is specifically sensitive to heatwave conditions, female is not. Spermatogenesis is disrupted by heat. Sperm function is damaged by heat in female storage. There are transgenerational impacts of heatwave conditions on offspring reproduction. Phenotypic plasticity among gametes enables some buffering against rapid thermal change within reproduction. There may be population consequences of this sensitivity under climate change. Final results have been published in Nature Comms and eLIFE, with major public and media engagement.
Exploitation Route Recognition of thermal reproductive sensitivity in ectothermic insects being one mechanism by which insect declines can be driven by climate change and extreme weather.

Management of insect pest in contained facilities using heat.
Sectors Agriculture, Food and Drink,Environment

URL https://natureecoevocommunity.nature.com/users/192562-matthew-gage/posts/41009-spermatozoal-sensitivity
 
Description Following publication in Nature Communications, and active media engagement, the work has raised the profile of climate change impacts on biodiversity, and possible routes for negative impacts.
First Year Of Impact 2018
Sector Agriculture, Food and Drink,Environment
Impact Types Societal

 
Description Media engagement following major publication 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Interviews for print, radio and TV media following publication of our Nature Communications paper 'Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect'. The publication achieved an exceptional Altmetric score of 600+ in its first week following publication. The PI engaged actively in all requests for engagement, including live interviews on radio stations across the world, print edition broadsheets and major online activity.
Year(s) Of Engagement Activity 2018
URL https://www.bbc.co.uk/news/science-environment-46194383