Final Report Summary - LIFHISBURBEE (Developmental programming and the costs of reproduction)
The costs of reproduction lie at the heart of life-history theory and their magnitude determines key biological processes, such as how rapidly animals age, the effort that parents devote to offspring care and the intensity of social conflicts. As individuals only have limited resources to cope with different body activities, reproduction trade-offs against somatic maintenance and repair, and prioritising allocation to one process inevitably means a shortfall to the other. For example, investing in current fecundity can lead to an increase in intrinsic mortality (through a decreased investment in maintenance of somatic tissue), a decrease in future fecundity (through a decreased investment in maintenance of reproductive tissue), or both. Thus, the nature and extent of these costs can vary widely: this has important implications for several key biological processes, and ultimately for the evolution of phenotypic plasticity in life histories.
There is growing evidence that the costs of reproduction are affected by the conditions experienced in very early life. Restricted resource intake during this critical developmental period can cause competition amongst different body tissues, with investment in some structures prioritised at the expense of others. Accordingly, tissues that are sacrificed during competition for development should senesce more rapidly in later life and be more vulnerable to damage associated with reproducing, thus magnifying the costs of reproduction. In many animal taxa, the main factor influencing the quality of the early developmental environment is the extent to which offspring are provisioned by parents. However, studies considering how the level of care received as an offspring affects the costs of reproduction sustained in later life are lacking. Using a multidisciplinary approach, incorporating experimental work in the laboratory and theoretical analyses, we aimed to investigate how the developmental environment in early life influences the costliness of reproduction, and the knock-on effects for senescence, parental care and social evolution. The experimental work included three main studies of the burying beetle Nicrophorus vespilloides. This species has complex biparental care and readily breeds under standardised laboratory conditions. Adults breed on small vertebrate carcasses which they defend from conspecifics and from microbial competitors, the latter being achieved by smearing the flesh with oral and anal exudates which contain antibacterial substances. Parents also constitute the primary source of nourishment of the larvae especially during the first hours after hatching, but offspring can self-feed and reach adulthood alone in case their parents are deserting.
In all studies, we first manipulated the quality of the developmental environment experienced by our experimental individuals by manipulating the duration of parental care received as larvae. To this end, we removed the fathers from all broods shortly before hatching to reduce the experimental noise in subsequent manipulations; then, we removed the mothers 0, 8 or 24 h after hatching, and added a control treatment where mothers reared their larvae until dispersal from the carcass. Experimental larvae from each of these four groups were subsequently set up to reach adulthood, and employed for one of the following experiments.
In experiment 1, we paired experimental males and females with a virgin adult of our stock population as soon as they reached sexual maturity, to let them start a breeding bout. After that, we removed the stock parents at hatching and assigned the experimental subjects either a small or a large brood of cross-fostered larvae from their maternal care duration treatment group, which they reared until dispersal. Then, we recorded breeding success and individual lifespan following the experimental breeding bout.
In experiment 2, we paired experimental females over two consecutive breeding bouts with a stock partner and assigned them either a carcass previously dipped in a solution laden with bacteria which increased the extent of microbial competition experienced at breeding, or a control carcass. Then, we widowed our females shortly before hatching, left them completing each breeding bout alone, and recorded their breeding success and lifespan following the experimental breeding bouts.
Finally, in experiment 3, we paired experimental females over two consecutive breeding bouts with the same stock partner, and left all pairs rearing their broods until dispersal. Then, we recorded the breeding success of each pair and individual lifespan following the experimental breeding bouts for both experimental females and their stock partners.
All three experiments demonstrated that experiencing a poor-quality environment during early life is detrimental for the future individual performance as adult: 0 and 8-h individuals generally showed lower breeding success and shorter lifespan than individuals that received prolonged maternal care as larvae, these differences being enhanced when they faced a harsher breeding context in the adulthood as in experiment 2. In addition, experiment 3 showed that poor quality females increase the costliness of reproduction also for their unmanipulated partners, as they reported both shorter lifespan and lower fecundity over the experimental breeding bouts compared with males paired with high quality females. Finally, experiment 1 showed that males invest less than females over postnatal care of the offspring, especially when they experienced a poor rearing environment during early life or face large broods at reproduction. Further evidence for sex-specific costs of tasks connected with parental care, and more in general, for sexual conflict among partners over reproduction emerged from two additional studies we performed on unmanipulated individuals from our stock colony. In particular, we found that males invested more during the preparation of the carcass and tended to reduce their contribution after hatching of the larvae, while females invested more on postnatal parenting. In addition, the reproductive costs to females were enhanced by the presence of their partner until the end of the breeding bout compared with a treatment where males were removed before hatchng, probably because widowed females are free to feed themselves on the carcass employed for breeding in order to recoup some of the costs they face during reproduction.
The theoretical work focussed on building state-dependent models to analyse how the quality of the early developmental environment influences the subsequent costliness of reproduction, and whether current fecundity trades off primarily with lifespan or future fecundity. In order to allow for independent variation in the rate of somatic and of reproductive deterioration, our approach featured two independent state variables that described accumulated damage to an individuals soma and reproductive capacity, the former influencing mortality, the latter fecundity, against a background of unpredictable variation in environmental conditions (as for example in experiment 2, see above). After several preliminary assays necessary to achieve the optimal modelling of each variable, our analyses are now almost and we expect to obtain finish them within a few weeks.
Overall, the project met its original objectives and clearly documented for the first time the effects of variation in the developmental environment, as represented by the quality of parental care received during early life, on individual life history. Our findings are relevant with respect to the study of key biological and evolutionary matters such as ageing, reproductive trade-offs, parental care, sexual conflict and social evolution and substantially enhance current knowledge in a capital area of worldwide behavioural and evolutionary ecology research.
There is growing evidence that the costs of reproduction are affected by the conditions experienced in very early life. Restricted resource intake during this critical developmental period can cause competition amongst different body tissues, with investment in some structures prioritised at the expense of others. Accordingly, tissues that are sacrificed during competition for development should senesce more rapidly in later life and be more vulnerable to damage associated with reproducing, thus magnifying the costs of reproduction. In many animal taxa, the main factor influencing the quality of the early developmental environment is the extent to which offspring are provisioned by parents. However, studies considering how the level of care received as an offspring affects the costs of reproduction sustained in later life are lacking. Using a multidisciplinary approach, incorporating experimental work in the laboratory and theoretical analyses, we aimed to investigate how the developmental environment in early life influences the costliness of reproduction, and the knock-on effects for senescence, parental care and social evolution. The experimental work included three main studies of the burying beetle Nicrophorus vespilloides. This species has complex biparental care and readily breeds under standardised laboratory conditions. Adults breed on small vertebrate carcasses which they defend from conspecifics and from microbial competitors, the latter being achieved by smearing the flesh with oral and anal exudates which contain antibacterial substances. Parents also constitute the primary source of nourishment of the larvae especially during the first hours after hatching, but offspring can self-feed and reach adulthood alone in case their parents are deserting.
In all studies, we first manipulated the quality of the developmental environment experienced by our experimental individuals by manipulating the duration of parental care received as larvae. To this end, we removed the fathers from all broods shortly before hatching to reduce the experimental noise in subsequent manipulations; then, we removed the mothers 0, 8 or 24 h after hatching, and added a control treatment where mothers reared their larvae until dispersal from the carcass. Experimental larvae from each of these four groups were subsequently set up to reach adulthood, and employed for one of the following experiments.
In experiment 1, we paired experimental males and females with a virgin adult of our stock population as soon as they reached sexual maturity, to let them start a breeding bout. After that, we removed the stock parents at hatching and assigned the experimental subjects either a small or a large brood of cross-fostered larvae from their maternal care duration treatment group, which they reared until dispersal. Then, we recorded breeding success and individual lifespan following the experimental breeding bout.
In experiment 2, we paired experimental females over two consecutive breeding bouts with a stock partner and assigned them either a carcass previously dipped in a solution laden with bacteria which increased the extent of microbial competition experienced at breeding, or a control carcass. Then, we widowed our females shortly before hatching, left them completing each breeding bout alone, and recorded their breeding success and lifespan following the experimental breeding bouts.
Finally, in experiment 3, we paired experimental females over two consecutive breeding bouts with the same stock partner, and left all pairs rearing their broods until dispersal. Then, we recorded the breeding success of each pair and individual lifespan following the experimental breeding bouts for both experimental females and their stock partners.
All three experiments demonstrated that experiencing a poor-quality environment during early life is detrimental for the future individual performance as adult: 0 and 8-h individuals generally showed lower breeding success and shorter lifespan than individuals that received prolonged maternal care as larvae, these differences being enhanced when they faced a harsher breeding context in the adulthood as in experiment 2. In addition, experiment 3 showed that poor quality females increase the costliness of reproduction also for their unmanipulated partners, as they reported both shorter lifespan and lower fecundity over the experimental breeding bouts compared with males paired with high quality females. Finally, experiment 1 showed that males invest less than females over postnatal care of the offspring, especially when they experienced a poor rearing environment during early life or face large broods at reproduction. Further evidence for sex-specific costs of tasks connected with parental care, and more in general, for sexual conflict among partners over reproduction emerged from two additional studies we performed on unmanipulated individuals from our stock colony. In particular, we found that males invested more during the preparation of the carcass and tended to reduce their contribution after hatching of the larvae, while females invested more on postnatal parenting. In addition, the reproductive costs to females were enhanced by the presence of their partner until the end of the breeding bout compared with a treatment where males were removed before hatchng, probably because widowed females are free to feed themselves on the carcass employed for breeding in order to recoup some of the costs they face during reproduction.
The theoretical work focussed on building state-dependent models to analyse how the quality of the early developmental environment influences the subsequent costliness of reproduction, and whether current fecundity trades off primarily with lifespan or future fecundity. In order to allow for independent variation in the rate of somatic and of reproductive deterioration, our approach featured two independent state variables that described accumulated damage to an individuals soma and reproductive capacity, the former influencing mortality, the latter fecundity, against a background of unpredictable variation in environmental conditions (as for example in experiment 2, see above). After several preliminary assays necessary to achieve the optimal modelling of each variable, our analyses are now almost and we expect to obtain finish them within a few weeks.
Overall, the project met its original objectives and clearly documented for the first time the effects of variation in the developmental environment, as represented by the quality of parental care received during early life, on individual life history. Our findings are relevant with respect to the study of key biological and evolutionary matters such as ageing, reproductive trade-offs, parental care, sexual conflict and social evolution and substantially enhance current knowledge in a capital area of worldwide behavioural and evolutionary ecology research.