Evolution of larval competitiveness and associated life‐history traits in response to host shifts in a seed beetle

Abstract

Resource competition is frequently strong among parasites that feed within small discrete resource patches, such as seeds or fruits. The properties of a host can influence the behavioural, morphological and life-history traits of associated parasites, including traits that mediate competition within the host. For seed parasites, host size may be an especially important determinant of competitive ability. Using the seed beetle, Callosobruchus maculatus, we performed replicated, reciprocal host shifts to examine the role of seed size in determining larval competitiveness and associated traits. Populations ancestrally associated with either a small host (mung bean) or a large one (cowpea) were switched to each other's host for 36 generations. Compared to control lines (those remaining on the ancestral host), lines switched from the small host to the large host evolved greater tolerance of co-occurring larvae within seeds (indicated by an increase in the frequency of small seeds yielding two adults), smaller egg size and higher fecundity. Each change occurred in the direction predicted by the traits of populations already adapted to cowpea. However, we did not observe the expected decline in adult mass following the shift to the larger host. Moreover, lines switched from the large host (cowpea) to the small host (mung bean) did not evolve the predicted increase in larval competitiveness or egg size, but did exhibit the predicted increase in body mass. Our results thus provide mixed support for the hypothesis that host size determines the evolution of competition-related traits of seed beetles. Evolutionary responses to the two host shifts were consistent among replicate lines, but the evolution of larval competition was asymmetric, with larval competitiveness evolving as predicted in one direction of host shift, but not the reverse. Nevertheless, our results indicate that switching hosts is sufficient to produce repeatable and rapid changes in the competition strategy and fitness-related traits of insect populations.

The interaction effect between intraspecific competition and seed quality on the life‐history traits of the seed‐feeding beetleAcanthoscelides macrophthalmus

“…However, after correcting for body size (i.e., specifying a particular body mass), the authors found that females produced larger eggs in the presence of competition, suggesting that they may produce larger eggs to increase larval survival despite their reduction in body mass. A recent study also conducted with C. maculatus showed that the changes in body size did not occur when beetles were reared on larger seeds, even though female fecundity increased (Fox & Messina, 2018). Here, our findings corroborate those for C. maculatus because differences in body size were not found for A. macrophthalmus despite the observed differences in fecundity.…”

“…A recent study also conducted with C. maculatus showed that the changes in body size did not occur when beetles were reared on larger seeds, even though female fecundity increased (Fox & Messina, ). Here, our findings corroborate those for C. maculatus because differences in body size were not found for A. macrophthalmus despite the observed differences in fecundity.…”

“…It has been shown that changes in the body size of bruchines can be related to the type of larval competition they exhibit. For example, when C. maculatus larvae grow on seeds of small and medium sizes, they exhibit aggressive behavior, which is characteristic of contest competitors (Messina, 1991;Fox & Messina, 2018). In that example, selection favored individuals with large bodies.…”

“…For example, when S. limbatus was fed using a host that caused higher larval mortality (i.e., a poor host), females laid larger and fewer eggs (Fox et al, 1997). On the other hand, when larger seeds were offered to C. maculatus (i.e., an environment of low competition) after host shifting, the females laid more but smaller eggs (Fox & Messina, 2018). However, it is interesting to note that this investment in egg size was, in our study, observed only in the absence of competition.…”

Dynamics of genomic change during evolutionary rescue in the seed beetleCallosobruchus maculatus

“…Lastly, some sources of selection could be density dependent. Male-male competition is common in high-density populations of C. maculatus (Hotzy & Arnqvist, 2009), and larvae from our Indian source population exhibit particularly strong contest competition within seeds (Messina, 1991; Fox & Messina, 2018).…”