Sexual signals such as colourful plumage are critical for mate attraction and hence reproduction, even though their conspicuousness exposes them to parasites and predators (Zuk & Kolluru 1998
). Such signals often represent compromises between natural and sexual selection. Since 1991, we have been examining the responses to such conflicting selective pressure in populations of the field cricket Teleogryllus oceanicus
, an Australian and Pacific Island species introduced to three Hawaiian Islands (Oahu, the Big Island of Hawaii and Kauai), where it is subject to an acoustically orienting parasitoid fly, Ormia ochracea
(Zuk et al. 1993
). The parasitoid is North American in origin and overlaps in range with T. oceanicus
only in Hawaii (Lehmann 2003
). The fly finds its host using the same signal (the calling song) that males produce to attract mates; fly larvae burrow into the cricket and develop inside, killing the host upon emergence.
Previous work demonstrated that parasitized populations have altered song structure, response to disturbance and calling behaviour compared with unparasitized populations (Zuk et al. 1993
; Rotenberry et al. 1996
; Lewkiewicz & Zuk 2004
). Here we document a much more extreme and rapid adaptive change, near-complete loss of calling, in the Kauai population, and examine its consequences for mate location and the evolution of mate choice in the context of interaction between behavioural plasticity and morphological adaptation.
Kauai has always had the highest prevalence of the parasitoid, with nearly 30% of calling males harbouring the fly (Zuk et al. 1993
). Presumably owing to the associated mortality, with each field visit since 1991 we heard and observed fewer crickets on that island, and in 2001 only heard a single calling male, with all crickets extremely scarce in intensive searches (methods; see electronic supplementary material). Over a three day visit in 2003, although we heard none calling, crickets were far more abundant than before in their habitat of fields and lawns. Further examination revealed that virtually all Kauai males had female-like wings, lacking the normal stridulatory apparatus of file and scraper required for sound production (hereafter called flatwings; ). Instead, the file is reduced in size and relocated at an angle precluding sound production (). Flatwings are thus unable to call. Populations from the other Hawaiian Islands as well as descendents from eggs collected on Kauai before 2003 continue to exhibit normal wings.
Figure 1 Underside of the right forewing from a normal-winged male (a), flatwing male (b) and female (c) Teleogryllus oceanicus. (d–f) SEM micrographs of these wings showing magnified structures of interest. Normal-winged males possess a stridulatory apparatus (more ...)
Loss of calling clearly protects the crickets from the parasitoid. Although flies are still attracted to sound traps on Kauai, out of 121 flatwings dissected, only one harboured parasitoid larvae, versus greater than 30% infestation rates previously associated with normal-winged males on Kauai. But this protection comes with the price of losing the sexual signal. How do females locate silent flatwing males? Moreover, like most field crickets, T. oceanicus
males produce a courtship song after a female is within close range. Females in this and other species require the male to produce the courtship song before mounting to receive a spermatophore (Burk 1983
; Libersat et al. 1994
). Flatwings can produce neither calling nor courtship song, and crickets are not known to use long-range pheromones for mate location (Tregenza & Wedell 1997
). Nevertheless, the now-thriving population of T. oceanicus
on Kauai suggests that the obstacles in both detecting and accepting mates have been overcome.
Here, we focus on the difficulty of long-range mate location. We propose that flatwing male T. oceanicus
on Kauai behave as ‘satellites’ (Cade 1980
) to the few calling males that remain, with an enhanced phonotaxis response to a calling song that brings them into close proximity with the caller. Attracted females should then be much more likely to encounter flatwings as potential mates than they would if the flatwings simply moved at random throughout the habitat. Male crickets from a variety of species, including T. oceanicus
, are normally attracted to the song of other males (Kiflawi & Gray 2000
), but they usually settle at least 1
m from the caller (M. Zuk 1991–2004, unpublished observations). Satellite behaviour was proposed for a related species, Gryllus texensis
, subject to parasitization by O. ochracea
in North America (Cade 1975
). We predicted that flatwings would move towards a caller more quickly, and stop at a point closer to the caller, than would normal-winged males.