Chemical basis of courtship in a beetle (Neopyrochroa flabellata): Cantharidin as "nuptial gift".

Abstract

The amount of cantharidin (Spanish fly) that the Neopyrochroaflabellata male presents to the female as a glandular offering during courtship represents only a small fraction of the total cantharidin the male accumulates systemically following ingestion of the compound. A major fraction of the acquired cantharidin is stored by the male in the large accessory glands of the reproductive system. At mating, the male transfers this supply, presumably as part of the sperm package, to the spermatheca of the female. The female in turn allocates the gift to the eggs. Eggs endowed with cantharidin proved relatively invulnerable to attack by a predaceous beetle larva (Coleomegilla maculata).We demonstrate here that the cantharidin ingested by male Neopyrochroa flabellata (1) is transferred in large measure to the female at mating, and by the female, for protective purposes, to the eggs. Specifically, we demonstrate that (i) cantharidin (Spanish fly), ingested by the male, accumulates primarily in the large accessory glands of the reproductive system; (ii) mating leads to appearance of cantharidin in the sperm receptacle (spermatheca) of the female; (iii) eggs sired by cantharidin-fed males contain cantharidin; and (iv) cantharidin-laden eggs, unlike cantharidin-free eggs, are protected against predation. Preliminary aspects of this study were reported earlier (2). MATERIALS AND METHODSSource and maintenance of beetles, chemical analyses for cantharidin content, and statistical analyses were as described (1). Values (including those in the figures) are given as mean ± SEM.Cantharidin Feeding. Males designated as cantharidin-fed (n = 58) were offered crystalline cantharidin as described (1). Total cantharidin offered to individuals ranged from 5 to 3050 ,ug, given over a span of 1-31 days. Mean quantity per beetle was 766 ± 83 ,ug, given over a period of 8.4 ± 0.9 days.Males designated as cantharidin-unfed (n = 34) were kept unexposed to cantharidin.Dissection. Beetles were killed by freezing and dissected under saline solution. Components of the male reproductive system that were analyzed for cantharidin content were (see Fig. 1A) as follows: testes, including the ducts leading to the seminal vesicles; seminal vesicles; large accessory glands; small accessory glands; and ejaculatory duct. Components of the female reproductive system that were analyzed were (see Fig. 1C) as follows: ovaries, spermatheca, and median oviduct. For both males and females, heads were also analyzed, as well as the alimentary canal, and a sample, designated as remains, consisting of all body parts, minus head, reproductive system, and gut. All samples were weighed immediately after dissection. A small fraction of samples was lost in the course of the analyses (sample sizes for component parts were therefore sometimes variable).Dissection of mated males (n = 7) and mated females (n = 9) was performed, respectively, within 1.0-3.5 h (2.6 ± 0.4 h) and 0.1-2.7 h (1.2 ± 0.3 h) after mating.Matings. These were staged in Petri dishes, as in the co...

Melatonin: a possible link between the presence of artificial light at night and reductions in biological fitness

“…The variation in female investment of melatonin may also explain the lack of observed variation in fecundity in the current experiment, as females were mated to males that were maintained under normal light conditions. Thus it is conceivable that male-derived melatonin transferred during mating was able to mitigate variation in female condition during egg-laying sensu the distasteful cantharidins transferred during mating by the male beetle, Neopyrochroa flabellate, which females then allocate to eggs, so providing them with protection from predation [96]. The fact that the effect of melatonin supplementation on immune function varied highlights the complexity of the underlying relationships between light, melatonin and life history traits.…”

Sexually transmitted chemical defense in a moth (Utetheisa ornatrix)

“…We predict, however, that the strategy will be shown to have counterparts in insects, where males so often transmit sizeable spermatophores to females (21). One can certainly imagine the strategy being at play in such insects as D. gilipus and N. flabellata, where seminal transfer of defensive chemicals has been established (15)(16)(17).…”

“…We ourselves had shown such chemical transfer to occur in a danaid butterfly, Danaus gilippus, where the male, as in Utetheisa, transmits PA that it sequesters from plants to the female (15), and in a pyrochroid beetle, Neopyrochroa flabellata, where the terpenoid toxin cantharidin is bestowed on the female (16,17). In all these cases, including Utetheisa, the assumption had been that the beneficiaries of the transfer are the offspring, and evidence did indeed indicate that the eggs of Utetheisa and N. flabellata derive protection from the PA or cantharidin they receive from their respective fathers (5, 17).…”

Active foraging for toxic prey during gestation in a snake with maternal provisioning of sequestered chemical defences

“…The focus of this study is the feeding ecology of parents in the context of defensive provisioning. Natural selection may favour those females that actively accumulate and endow their offspring with more defensive chemicals when the concentration has an effect on offspring survival [3,[7][8][9]. Although a study has reported mating-induced behavioural switching in females of a firefly, which is likely to facilitate acquisition of toxins used for chemical protection of offspring [14], few studies have addressed natural behaviour related to acquisition of defensive chemicals.…”

“…In certain groups of insects, the mechanism and ecology of chemical protection of offspring have received much attention (e.g. [3,[7][8][9]), but there is comparatively little research on vertebrate systems, even though examples of vertebrate species that produce unpalatable or poisonous offspring are increasing [4,6,10].…”