Individual plastic responses by males to rivals reveal mismatches between behaviour and fitness outcomes

Abstract

Plasticity in behaviour is of fundamental significance when environments are variable. Such plasticity is particularly important in the context of rapid changes in the socio-sexual environment. Males can exhibit adaptive plastic responses to variation in the overall level of reproductive competition. However, the extent of behavioural flexibility within individuals, and the degree to which rapidly changing plastic responses map onto fitness are unknown. We addressed this by determining the behaviour and fitness profiles of individual Drosophila melanogaster males subjected to up to three episodes of exposure to rivals or no rivals, in all combinations. Behaviour (mating duration) was remarkably sensitive to the level of competition and fully reversible, suggesting that substantial costs arise from the incorrect expression of even highly flexible behaviour. However, changes in mating duration matched fitness outcomes (offspring number) only in scenarios in which males experienced zero then high competition. Following the removal of competition, mating duration, but not offspring production, decreased to below control levels. This indicates that the benefit of increasing reproductive investment when encountering rivals may exceed that of decreasing investment when rivals disappear. Such asymmetric fitness benefits and mismatches with behavioural responses are expected to exert strong selection on the evolution of plasticity.

Experience of mating rivals causes males to modulate sperm transfer in the fly Drosophila pseudoobscura

“…Nevertheless, under the same experimental design as we use here, there is no correlation between mating duration and offspring number in D. melanogaster ). In addition, in D. melanogaster, the behavioural response (increase in mating duration) and the fitness consequences (offspring number in the first 24 h) can become uncoupled (Bretman et al, 2012). That is, over successive matings and switches between exposure or not to a rival, males match their behaviour to the most recently experienced environment, but the number of offspring does not necessarily follow the behaviour.…”

Social context-dependent modification of courtship behaviour in Drosophila prolongata

“…For example, in the presence of rivals, courtship intensity is enhanced in crickets [3] and fighting fish [4], or the duration of copulation is extended in fruit flies [5,6] and soldier flies [7]. In these cases, males increase their investment in reproduction.…”

Flexible memory controls sperm competition responses in maleDrosophila melanogaster

“…All wild type flies were the Dahomey strain as in our previous studies [3,9,11,20]. Wild type larvae were raised at a standard density of 100 per vial.…”