Anticipatory flexibility: larval population density in moths determines male investment in antennae, wings and testes

Abstract

Developmental plasticity provides individuals with a distinct advantage when the reproductive environment changes dramatically. Variation in population density, in particular, can have profound effects on male reproductive success. Females may be easier to locate in dense populations, but there may be a greater risk of sperm competition. Thus, males should invest in traits that enhance fertilization success over traits that enhance mate location. Conversely, males in less dense populations should invest more in structures that will facilitate mate location. In Lepidoptera, this may result in the development of larger antennae to increase the likelihood of detecting female sex pheromones, and larger wings to fly more efficiently. We explored the effects of larval density on adult morphology in the gum-leaf skeletonizer moth, , by manipulating both the number of larvae and the size of the rearing container. This experimental arrangement allowed us to reveal the cues used by larvae to assess whether absolute number or density influences adult responses. Male investment in testes size depended on the number of individuals, while male investment in wings and antennae depended upon larval density. By contrast, the size of female antennae and wings were influenced by an interaction of larval number and container size. This study demonstrates that male larvae are sensitive to cues that may reveal adult population density, and adjust investment in traits associated with fertilization success and mate detection accordingly.

Integrative developmental ecology: a review of density-dependent effects on life-history traits and host-microbe interactions in non-social holometabolous insects

“…While apyrene sperm is not capable of fertilising eggs it may nonetheless affect egg fertilisation in sperm competitive contexts (Silberglied et al 1984;Watanabe 2016). Similarly, in the gum-leaf skeletonizer moth Uraga lugens, males from high larval densities invest more in testis size but have relatively shorter wing and antenna length, revealing a tradeoff between investing in finding mates versus winning paternity (Johnson et al 2017). Female antenna and wing sizes are density-independent or social-dependent, respectively, which uncovers sex-specific responses to population density at the larval stage (Johnson et al 2017).…”

Evolution of male antennal size in moths (Lepidoptera): a comparative test of potential trade‐offs and correlated growth in Australian species

“…These trade-offs may manifest themselves as trade-offs between pre-copulatory and post-copulatory traits, the exact degree of which potentially depends on specific environmental conditions: males of moths that are raised at low population densities tend to develop relatively larger antennae, indicating greater investment in mate detection and location when mates are scarce (pre-copulatory strategies), while those raised at high population densities grow relatively larger testes and have higher sperm counts, indicating investment in traits that ensure a male sires a higher proportion of offspring when sperm competition is likely to be greater (paternity protectiona post-copulatory strategy) (Gage 1995;Johnson et al 2017b). The relationship between testis size and antennal size may not be consistent across species.…”

Sexual selection and organs of sense: Darwin’s neglected insight

“…Studies of anticipatory life-history investment also provide insights into the costs of receptor organ development. Adult males of the leaf skeletoniser moth Uraba lugens Walker, 1866 that were raised as larvae in high densities had smaller antennae (but larger testes) than those reared at a low density, presumably because it is easier to locate a mate when the adult population is dense, but this also increases the risk of sperm competition (Johnson et al, 2017a). This anticipatory flexibility in sensory investment may explain why there was no evolutionary response in antennal morphology to long-term selection through population density in the Indian meal moth Plodia interpunctella Guenée, 1845(Ashman et al, 2016.…”