Date Published: April 23, 2019
Publisher: Public Library of Science
Author(s): Virve Sõber, Siiri-Lii Sandre, Toomas Esperk, Tiit Teder, Toomas Tammaru, Matjaž Kuntner.
Sex-specific mechanisms of the determination of insect body sizes are insufficiently understood. Here we use the common heath moth, Ematurga atomaria (Lepidoptera: Geometridae) to examine how larval growth trajectories differ between males and females. We monitored the development of 1379 larvae in controlled laboratory conditions. Sexually dimorphic development times during the first four instars were associated with sexual size dimorphism (SSD) in the beginning of the fifth (last) instar, when females were on average 15% heavier than males. Similarly, the duration of the last instar was about 13% longer in females. Further, we specifically focussed on the estimates of differential (instantaneous) growth rates of the larvae based on 24h mass increments of the 2nd, 3rd, 4th and 5th day in the beginning of the last instar. We calculated ‘allometric’ differential growth rates as the per-day increase in cube-root-transformed mass of the larvae. We found that allometric growth rates were slightly but significantly larger in females than in males. As this measure of growth rate (in contrast to the relative growth rate, based on the ratio of masses recorded at consecutive measurements) did not depend on body size, it allows an unambiguous separation of the effects of sex and size. We conclude that in accordance with an emerging general pattern, larger female body size in E. atomaria is achieved primarily by means of a longer growth period. Furthermore, our study shows that the differential growth rate can also be sexually dimorphic and contribute to SSD. This contribution, however, is lower than that of the development time by an order of magnitude. In addition to development periods and growth rates, other parameters of the non-linear growth curves of insect larvae also need to be considered in the context of SSD determination. In particular, weight loss prior to pupation was shown to be considerably larger in females than in males.
Sexual differences in body size (sexual size dimorphism, SSD) are a widespread phenomenon in most animal groups [1, 2]. Females are the larger sex in most invertebrates [3, 4, 5] and poikilothermic vertebrates [6, 7], whereas male-biased SSD is typical of birds [8, 9] and mammals [10, 11]. Evolutionary explanations of sexual size dimorphism primarily rely on selective forces operating in the adult stage. Fecundity selection is generally considered to cause female-biased SSD [4, 12, 13], but see , whereas male-biased size dimorphism is explained by sexual selection [1, 15, 16] but see . Importantly, however, also the non-reproductive life stages may have a contribution. For example, sexual dimorphism may be affected by natural selection operating during the juvenile development. Such selective forces on growth schedules per se must depend on the proximate patterns and mechanisms of juvenile growth . Ontogenetic mechanisms leading to sex-related differences in body size remain, however, insufficiently understood, which may result in an incomplete understanding of the selective factors that have shaped SSD (for insects, see however [19, 20].
Sex-related differences in growth patterns were present both before and during the last (5th) instar of E. atomaria larvae. Female-biased SSD could be observed already in the beginning of the last instar (Table 1): on average, the female larvae were about 1.15 times the mass of the male larvae at that time. The higher initial mass of females at the beginning of 5th instar was coupled with growing for a longer time during the first four instars: for females, it took on average a day (4.5%) longer to grow from hatching from the egg until the beginning of the 5th instar (Table 1); egg size is not sexually dimorphic in E. atomaria (M. Martverk, unpublished).
In the studied moth, sexual size dimorphism (SSD) appears to be associated, along with other mechanisms discussed below, with the longer growing time of the larger sex. The average body mass of the female larvae, being coupled with longer development periods over the first 4 instars, was higher than that of the male larvae by the end of the penultimate instar. Females grew for a longer time than males also during their last instar. The fact that SSD did not increase in the course of the last instar (the females were about 1.16 times heavier both in the beginning of the last instar, and as pupae) could be interpreted as questioning the causal connection between longer development time and larger sizes. However, the positive association between mass gain and development time was observed also when the period from the beginning of the last instar until achieving mass maximum (higher in females) was considered.