An operating cost of learning in Drosophila melanogaster

Abstract

Although the fitness benefits of learning are well understood, we know little about its costs; yet both are essential to understand the evolution of animal learning. We tested the hypothesis that learning has an operating cost, such that an animal repeatedly forced to use its learning ability would show a reduction in some fitness component(s), relative to an animal of the same genotype that does not have to learn. Five 'High-learning' lines of Drosophila melanogaster, which had been selected for improved learning ability, were exposed to 12 consecutive 48-h cycles of alternating conditioning treatment under mild nutritional stress. Their learning score first increased, reaching a maximum around day 12 (i.e. the sixth conditioning cycle), and then progressively declined. These changes were not due to ageing, as they were not observed in flies from the same lines maintained under standard conditions. From around day 12, the productivity (egg-laying rate) of the flies in the conditioning treatment became progressively reduced, relative to flies from the same lines not exposed to conditioning, but otherwise kept under the same food-limited conditions. This reduction in productivity was not observed when these treatments were applied to five 'Low-learning' lines, which had not been exposed to selection, and which show no detectable response to conditioning under our experimental conditions. Furthermore, exposure to repeated cycles of conditioning revealed an apparent trade-off between the learning score and productivity among the 'High-learning' lines. These results indicate an operating cost of learning, paid only by genotypes that show learning, rather than general effects of stress caused by the conditioning regime. Potential proximate explanations include (1) the impairment of oviposition decisions caused by the accumulation of memory interference and (2) energy costs of collecting, processing and storing information.

Phenotypic and genomic plasticity of alternative male reproductive tactics in sailfin mollies

“…This cost of plasticity per se is one of the avenues through which costs can limit the evolution of plasticity [29,32]. Reviews of the cost of plasticity [26,27] have found limited evidence for this type of cost because few studies have been designed to find it; there is little relevant information outside of model systems [67] and few studies of the cost of behavioural plasticity in contexts other than learning [68][69][70]. Our results suggest that there are transcriptional costs of behavioural plasticity and that it is possible to estimate the magnitude of these costs in a variety of empirical systems.…”

Interspecific and intersexual learning rate differences in four butterfly species

“…longer-lived butterflies should repeatedly employ their learning abilities, enabling them to gain more benefits than costs of learning. Such costs of learning have been reported in fruit flies, whereby flies from lines selected for improved learning ability had reduced larval competitive ability (Mery and Kawecki, 2003), lower egg-laying rates (Mery and Kawecki, 2004) and decreased lifespan (Burger et al, 2008) compared with flies from unselected lines.…”

Natural polymorphism affecting learning and memory in Drosophila

“…Thus, even though our understanding of ecological aspects of learning in fruit flies is still rudimentary, there is evidence that it contributes to their fitness under natural conditions. This would explain why Drosophila are capable of learning, despite learning ability being a costly adaptation (2,3,51). But is the effect of for polymorphism on learning and memory ecologically relevant?…”