Food is often a limiting factor for animals and an object of intense competition. In particular, competition for a limited amount of high quality food is likely to favour monopolization of resources through territoriality or social dominance as well as faster feeding and development. However, malnutrition may also result from food being of poor quality even if available in large amount. This type of nutritional stress may favour different adaptations than competition for high-quality food, such as efficient food processing and utilization.

Adaptation to both types of nutritional stress has been addressed with experimental evolution in Drosophila, where larvae in nature develop on ephemeral food patches of varying quality and often compete with other larvae [1], [2]. Experimental populations of D. melanogaster maintained under high larval density on high-quality food have evolved accelerated development, faster growth and increased competitive ability for food [3], [4]. This increased competitive ability, quantified as relative survival to adulthood of two strains competing for a small amount of food, appears to trade-off with lower energetic efficiency. This trade-off raises the question of whether greater competitive ability would also be favoured under nutritional stress resulting from low food quality rather than quantity, where the efficiency of food use might be more important than the scramble competition.

Here we address this question using six D. melanogaster populations adapted to chronic larval malnutrition as a result of being maintained for 84 generations under low density on an extremely poor larval food [5]. Similar to populations adapted to larval crowding, these populations have evolved faster development [5]. However, faster development does not automatically lead to competitive advantage [6]. Furthermore, in contrast to the crowding-adapted populations [3], [4], these populations do not show faster growth than unselected controls under good food conditions [7]. The question of their competitive ability thus remains open. Larval competitive ability in Drosophila is thought to be mediated to a significant degree by a higher feeding rate [8], [9]. Consistent with this, the experimental evolution of higher competitive ability in crowded populations has been coupled with an increase in larval feeding rate [4], [9], [10]. Conversely, larvae from populations selected for faster development [11], [12], [13] and parasitoid resistance [14], [15] have evolved both lower larval competitive ability and lower rates of larval feeding. Finally, fast-feeding D.melanogaster larvae from a bi-directional selection experiment on larval feeding rate were better competitors than both slow-feeding larvae and unselected controls [16]. Under scramble competition for high-quality food, a high feeding rate allows the individual to obtain more food before it is consumed by competitors. However, a higher rate of food intake might also be favoured in the absence of competition as a way to compensate for low nutritional content of food. Therefore, we also test if larvae from the selected populations show a higher rate of food intake than controls, and if variation in food intake and competitive ability correlates across replicate populations within selection regimes.

Despite the “tester” competitor sepia having a head-start, larvae from both regimes survived better than the “testers”, as indicated by positive values of competitive index. The competitive index was greater for larvae from selected than control populations (F_1,10 = 11.2, P = 0.007; Fig. 1A), while variation among the replicate populations was not significant (F_10,108 = 0.9, P = 0.54). However, the proportion of individuals surviving to adulthood did not differ between the regimes (selected 0.525±0.028, control 0.538±0.032; χ²₁ = 0.2, P = 0.64). Rather, the difference in competitive index was largely due to the lower survival of the tester sepia larvae when competing with the selected versus control lines (0.306±0.021 versus 0.362±0.020; χ²₁ = 9.3, P = 0.0022).

The amount of coloured yeast ingested by the larvae in 15 minutes, measured as OD was not different between the selection regimes (F_1,10 = 0.3, P = 0.6), but varied among replicate populations (F_10,23 = 4.7, P = 0.001) (Fig. 1B). There was a trend within both regimes for populations with higher feeding rates to have lower competitive ability (Fig. 1C). While suggesting a negative relationship between larval competitive ability and feeding rate (slope −0.17), this trend was not significant (F_1,9 = 2.9, P = 0.13); the significant difference in competitive index between selection regimes was confirmed (F_1,9 = 13.2, P = 0.005).

We found no differences in the wet weight of larvae at the time of feeding rate assays between selected (0.62±0.01 µg) and control populations (0.64±0.17 µg; F_1,10 = 0.8, P = 0.39), or among replicate populations (F_10,24 = 1.8, P = 0.12).

Over 84 generations of selection the study populations have been evolving under low-quality but relatively abundant food; under the selection regime the total energy content of food available per larva was about 10 times the energy content of a pre-pupation larva [23]. Yet, this study shows that these selected populations have evolved a stronger ability to compete for a very limited amount of high-quality food, which represents a very different type of nutritional stress. Enhanced competitive ability in Drosophila has so far only been reported from populations evolved under crowded conditions [3], [4]. In contrast, several other experimental selection regimes – for fast development [6], resistance to pathogens [19] and parasitoids [14], [15], or improved associative learning [24] – have led to a decrease in the competitive ability. Thus, our results are rather unexpected and suggest that the previously reported trade-off between competitive ability and energetic efficiency [4] has been of little importance in our selected populations.

It remains an open question whether the improved competitive ability was directly under selection under the poor food regime, despite the low density, or whether it is a by-product of evolutionary changes in other traits. The selected populations have evolved a smaller critical size for pupation initiation and complete pupation at substantially smaller size [7], and so they would presumably need less energy and nutrients to survive to adulthood. However, this does not explain their higher competitive index – they do not survive better in the competitive assays than the control populations. Rather, larvae from the selected populations exert stronger negative effects than controls on survival of the tester genotype. A potential explanation of this result would have been a higher rate of food consumption by larvae from the selected versus control populations, leaving less food for the tester larvae. However, the selected populations did not show consistently higher rates of food intake than controls, and the correlation among populations between food intake rate and competitive index tended to be negative. This is another unexpected result – previous studies found a close association between feeding rate and competitive ability (see Introduction).

We can thus only speculate about the mechanism of the stronger competitive impact of the larvae from the selected lines on the testers. The number of larvae surviving to adulthood did not differ between the selected and control populations. Nonetheless, among the larvae that did not survive, those from selected populations might have died later than those from the control populations. If so, the sepia larvae competing with larvae from a selected population would have transiently faced a larger number of competitors. However, other factors such as differences in foraging behaviour (e.g., the ability to find the best remaining microsites in the food paste), the time spent not feeding (e.g., wandering or moulting), toxicity or waste products or direct antagonistic interactions might have also contributed to this result.

Irrespective of the underlying mechanism, this study shows that a greater ability to compete for a limited amount of high-quality food may be favoured under chronic malnutrition at a rather low population density. Furthermore, it indicates that a higher competitive ability in Drosophila larvae can be decoupled from the rate of food intake. Finally, these results suggest that adaptive evolutionary change under some experimental regimes may be most readily apparent by examining effects on the fitness of competitors rather than that of the focal individuals.