Sexual selection in true fruit flies (Diptera:Tephritidae): transcriptome and experimental evidences for phytochemicals increasing male competitive ability

Abstract

In male tephritid fruit flies of the genus Bactrocera, feeding on secondary plant compounds (sensu lato male lures = methyl eugenol, raspberry ketone and zingerone) increases male mating success. Ingested male lures alter the male pheromonal blend, normally making it more attractive to females and this is considered the primary mechanism for the enhanced mating success. However, the male lures raspberry ketone and zingerone are known, across a diverse range of other organisms, to be involved in increasing energy metabolism. If this also occurs in Bactrocera, then this may represent an additional benefit to males as courtship is metabolically expensive and lure feeding may increase a fly's short-term energy. We tested this hypothesis by performing comparative RNA-seq analysis between zingerone-fed and unfed males of Bactrocera tryoni. We also carried out behavioural assays with zingerone- and cuelure-fed males to test whether they became more active. RNA-seq analysis revealed, in zingerone-fed flies, up-regulation of 3183 genes with homologues transcripts to those known to regulate intermale aggression, pheromone synthesis, mating and accessory gland proteins, along with significant enrichment of several energy metabolic pathways and gene ontology terms. Behavioural assays show significant increases in locomotor activity, weight reduction and successful mating after mounting; all direct/indirect measures of increased activity. These results suggest that feeding on lures leads to complex physiological changes, which result in more competitive males. These results do not negate the pheromone effect, but do strongly suggest that the phytochemical-induced sexual selection is governed by both female preference and male competitive mechanisms.

Close‐distance courtship of laboratory reared Bactrocera tryoni (Diptera: Tephritidae)

“…Wing movements have also been observed as a part of courtship dances in tephritids such as Anastrepha suspensa (Loew) (Sofian-Azirun et al 2011), Rhagoletis completa Cresson (Bush 1966) and Rhagoletis juglandis Cresson (Alonso-Pimentel et al 2000). If the former, this is evidence for synchronous supination being a key element in the mating process because all other behaviours are not significantly different; if the latter, this supports the hypothesis of mating success being directly proportional to male metabolic rate (Kumaran et al 2014b). The increased frequency of wing display by successful males may enhance recognition by females, thus increasing the chance of copulation.…”

“…During the crepuscular period, males initiate wing fanning (Mankin et al 2008), accompanied by release of a pheromone (Bellas & Fletcher 1979;Kumaran et al 2014a). Bactrocera tryoni females accept males, or reject them by pushing them off with their hind legs before copulation starts (Barton-Browne 1957; Kumaran et al 2014b); males commence copulation if not rejected by the female (Tychsen 1977;Weldon 2005). Bactrocera tryoni females accept males, or reject them by pushing them off with their hind legs before copulation starts (Barton-Browne 1957; Kumaran et al 2014b); males commence copulation if not rejected by the female (Tychsen 1977;Weldon 2005).…”

Sexual inhibition of female Queensland fruit flies mated by males treated with raspberry ketone supplements as immature adults

“…RK fed to immature males does not appear to simply persist in the body to later act directly on mature adults in a manner directly analogous to the action of cuelure or zingerone fed to mature males. This is not unexpected, given that even when fed to mature adult Q‐fly males the physiological effects of cuelure and zingerone on sexual performance only last 1 ‐ 3 days (Kumaran, Hayes et al., ; Kumaran, Prentis et al., ). Rather than modifying mating performance at the mature stage, the effects of RK fed to immature males appear to be mostly in accelerated development.…”

Raspberry ketone supplement promotes early sexual maturation in male Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)

“…Mature male oriental fruit flies exhibit substantially elevated sexual activity (wing fanning associated with pheromone calling) after feeding on ME, and melon flies exhibit substantially elevated sexual activity after feeding on cuelure . In Qfly, mature males that have fed on zingerone exhibit increased locomotion, and mounting attempts are more likely to result in copulation . Interestingly, while mature male Qflies gain similar sexual advantages from feeding on either cuelure or zingerone and show similar increases in activity levels, pheromones are rendered more attractive to females after feeding on cuelure but not after feeding on zingerone .…”