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

点击翻译按钮获取中文摘要

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.