Adaptation to larval crowding in Drosophila ananassae and Drosophila nasuta nasuta: increased larval competitive ability without increased larval feeding rate

Abstract

The standard view of adaptation to larval crowding in fruitflies, built on results from 25 years of multiple experimental evolution studies on Drosophila melanogaster, was that enhanced competitive ability evolves primarily through increased larval feeding and foraging rate, and increased larval tolerance to nitrogenous wastes, at the cost of efficiency of food conversion to biomass. These results were at odds from the predictions of classical K-selection theory, notably the expectation that selection at high density should result in the increase of efficiency of conversion of food to biomass, and were better interpreted through the lens of α-selection. We show here that populations of D. ananassae and D. n. nasuta subjected to extreme larval crowding evolve greater competitive ability and pre-adult survivorship at high density, primarily through a combination of reduced larval duration, faster attainment of minimum critical size for pupation, greater time efficiency of food conversion to biomass and increased pupation height, with a relatively small role of increased urea/ammonia tolerance, if at all. This is a very different suite of traits than that seen to evolve under similar selection in D. melanogaster, and seems to be closer to the expectations from the canonical theory of K-selection. We also discuss possible reasons for these differences in results across the three species. Overall, the results reinforce the view that our understanding of the evolution of competitive ability in fruitflies needs to be more nuanced than before, with an appreciation that there may be multiple evolutionary routes through which higher competitive ability can be attained.

Evolution of increased adult longevity in Drosophila melanogaster populations selected for adaptation to larval crowding

“…Taken together, the results of Archana (2010), Sarangi et al (2015) and our study show that adaptation to larval crowding can occur through more than one set of mechanisms. Such alternative mechanisms of adaptation to crowding have been detected by multiple other studies (Joshi & Thompson, 1995;Joshi et al, 2001;Dey et al, 2012;Nagarajan et al, 2014). We now address each of our results individually and then discuss the possible reasons that might have led to the evolution of a different set of mechanisms in our populations.…”

“…Thus, the mechanisms that underlie adaptations to larval crowding in the populations of Archana (2010) and Sarangi et al (2015) are very different from those found in the populations of Mueller et al (1993). Therefore, as suggested by other studies (Joshi & Thompson, 1995;Joshi et al, 2001;Dey et al, 2012;Nagarajan et al, 2014), there are multiple ways of adapting to larval crowding. Since in D. melanogaster, the larva is the chief feeding stage and larval resource acquisition plays a very important role in determining adult fitness components (Chippindale et al, 1993), it is quite possible that in the populations of Archana (2010), a very different suite of adult traits has evolved as a correlated response to selection (compared to the adult traits in the previous studies).…”

“…The outcomes of density-dependent selection have been explored in great detail by two sets of laboratory experimental evolution studies using D. melanogaster: studies on the r and K populations (Mueller & Ayala, 1981), and the CU and UU populations (Mueller et al, 1993), respectively. The results from these two sets of studies (reviewed in Nagarajan et al, 2014) show that laboratory populations of D. melanogaster selected for adaptation to larval crowding consistently evolve a set of larval traits including increased larval competitive ability (Mueller, 1988), larval feeding rates (Joshi & Mueller, 1988, 1996, locomotor activity during feeding (Sokolowski et al, 1997), urea tolerance (Borash & Ho, 2001), growth rate during post-critical size period (Santos et al, 1997) and minimum food requirement for pupation (Mueller, 1990;Joshi & Mueller, 1996). Theories, both verbal and formal, suggest that density-dependent selection can also affect the evolution of adult lifespan.…”

Local adaptation to developmental density does not lead to higher mating success in Drosophila melanogaster

“…Rib o et al, 1989;Shenoi et al, 2016) show that the reproductive (adult) phase of D. melanogaster can be greatly affected by the developmental (larval) phase. Larval density affects adult life-history traits like body size (Miller & Thomas, 1958;Nagarajan et al, 2016), fecundity (Alpatov, 1932;Pearl, 1932), lifespan (Miller & Thomas, 1958;Economos & Lints, 1984;Zwaan et al, 1991) and reproductive success (Rib o et al, 1989). Males that develop under low larval density emerge as larger individuals, have higher mating success, mate at a faster rate and remate more often compared to smaller males that emerge from crowded cultures (Partridge & Farquhar, 1981, 1983Partridge et al, 1987a, b;Turiegano et al, 2013;Wigby et al, 2015).…”

Intergenerational paternal effect of adult density inDrosophila melanogaster

“…In essence, density often determines the nature and intensity of selection acting on a population and has been studied within the broader premises of density dependent selection (MacArthur Wilson, 1967;Mueller, 1997;. Much of the existing literature investigated adaptation to increased (but stable) juvenile or adult density, using experimental evolution on laboratory populations of D. melanogaster (Mueller, Guo, & Ayala, 1991;Mueller & Sweet, 1986;Nagarajan, Natarajan, Jayaram, & Joshi, 2016;Sarangi, Nagarajan, Dey, Bose, & Joshi, 2016;. However, little is known about adaptation to fluctuating density.…”