Asymmetries in the fecundity, reproductive effort, and body size–fecundity relationship between asexual and sexual generations: An important step in understanding the evolution of heterogony

Background/Question/Methods Heterogony is a complex life cycle that involves alternation of sexual and asexual generations (cyclical parthenogenesis) to complete a bivoltine life cycle. Heterogony and its variations (loss of the sexual or asexual generation) characterize life cycles of cynipid gall-forming wasps. Little is known about the ecological forces that maintain or promote life cycle evolution in heterogonous species. Belonocnema treatae (Hymenoptera: Cynipidae) exhibits cyclical parthenogenesis on its host plant, live oak, Quercus fusiformis. Temporally segregated sexual and asexual generations develop, respectively, in multi-chambered root galls and single-chambered leaf galls. We examined body size and immediate correlates of each generation: leaf gall diameter (asexual generation) and number of siblings in root galls (sexual generation). We then determined the relationships among body size, potential fecundity, egg volume, and total reproductive effort via dissection of females for each generation. These data allowed us to (a) determine whether body size and fecundity can be predicted based on gall diameter for the asexual generation and number of siblings within galls of the sexual generation; (b) test the hypothesis that the body size–fecundity relationship scales equivalently between generations; and (c) test the hypothesis that the “cost of sex” (i.e., the 2x advantage of asexual reproduction) will be countered by increased body size and increased fecundity of the sexual generation. Results/Conclusions Body size correlated with gall size in the asexual (r = 0.53; P < 0.0001) but not the sexual generation, which indicated that variation in resource acquisition influenced asexual generation body size but did not support the hypothesis that sexual generation wasps compete for resources in variable-size root galls. Gall size predicted fecundity in the asexual (P < 0.0001) but not the sexual generation. Body size and potential fecundity were positively related in both generations (P < 0.0001), but the slope of the regressions differed among generations (P < 0.0001), indicating that selection has modified the relationship independently in each generation. Whereas egg shape differed between the generations (P < 0.0001), egg volume scaled equivalently with body size between the generations. The “cost of sex” was clearly exceeded in the sexual generation, as on average sexual generation females produced four times the number of eggs and six times the reproductive effort as did the asexual generation. These data allow us to make predictions of the direction and potential ecological forces that have driven the evolution of heterogony in this insect species.