Nagalingam Kumaran

Evolution of lure response in tephritid fruit flies: phytochemicals as drivers of sexual selection

The males of many Bactrocera species (Diptera: Tephritidae) respond strongly and positively to a smallnumber of plant-derived chemicals (¼ male lures). Males that have imbibed the lures commonly havea mating advantage over unfed males, but no female benefits have been demonstrated for femalesmating with lure-fed males. It has been hypothesized that the strong lure response is a case of runawayselection, where males receive direct benefits and females receive indirect benefits via ‘sexy sons’,ora case of sensory bias where females have a lower threshold response to lures. To test these hypotheseswe studied the effects of lure feeding on male mating, remating and longevity; while for females that hadmated with lure-fed males we recorded mating refractoriness, fecundity, egg viability and longevity. Weused Bactrocera tryoni as our test animal and as lures the naturally occurring zingerone and chemicallyrelated, but synthetic chemical cuelure. Feeding on lures provided direct male benefits in greater matingsuccess and increased multiple mating. For the first time, we recorded direct female effects: increasedfecundity and reduced remating receptivity. Egg viability did not differ in females mated with lure-fed orunfed males. The life span of males and females exposed to lures was reduced. These results reveal direct,current-generation fitness benefits for both males and females, although the male benefits appeargreater. We discuss that while lure response is indeed likely to be a sexual selection trait, there is no needto invoke runaway selection to explain its evolution. 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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

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 flys 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.

Indirect effects of phytochemicals on offspring performance of Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)

Phytochemical lures such as methyl eugenol (ME) and cue‐lure are used in the management of Bactrocera fruit flies for monitoring and control. These lures are not just attractants, but also trigger physiological changes in males that lead to enhanced mating success. Additionally, in the cue‐lure‐responsive Bactrocera tryoni, females mated with lure‐fed males exhibit changes in fecundity, remating receptivity and longevity. While the lures show current generation effects, no research has been carried out on possible multigenerational effects, although such effects have been hypothesized within a ‘sexy‐son’ sexual selection model. In this study, we test for indirect, cross‐generational effects of lure exposure in F1offspring of B. tryoni females mated with cue‐lure‐fed, zingerone‐fed and lure‐unfed (=control) males. The F1 attributes we recorded were immature development time, immature survival, adult survival and adult male lure foraging. No significant differences were found between treatments for any of the three life‐history measurements, except that the offspring sired by zingerone‐fed males had a longer egg development time than cue‐lure and control offspring. However, indirect exposure to lures significantly enhanced the lure‐foraging ability of F1 adult males. More offspring of cue‐lure‐fed males arrived at a lure source in both large flight cages and small laboratory cages over a 2‐h period than did control males. The offspring of zingerone‐fed males were generally intermediate between cue‐lure and control offspring. This study provides the first evidence of a next generation effect of fruit fly male lures. While the results of this study support a ‘sexy‐son’ sexual selection mechanism for the evolution of lure response in Bactrocera fruit flies, our discussion urges caution in interpreting our results in this way.

Genomic Resources Notes accepted 1 December 2013 – 31 January 2014

This article documents the public availability of (i) transcriptome sequence data, assembled and annotated contigs and unigenes, and BLAST hits from the Queensland fruit fly, Bactrocera tryoni; (ii) 75 single‐nucleotide variants (SNVs) from 454 sequencing of reduced representation libraries for Phalangiidae harvestmen, Megabunus armatus, Megabunus vignai, Megabunus lesserti, and Rilaena triangularis; and (iii) expressed sequence tags from 454 sequencing of the lepidopterans Lymantria dispar and Lymantria monacha.