Male Field Cricket Song Reflects Age, Allowing Females to Prefer Young
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Animal Behaviour xxx (2010) 1e11 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav Male field cricket song reflects age, allowing females to prefer young males L. Verburgt*, M. Ferreira, J.W.H. Ferguson Department of Zoology and Entomology and Centre for Environmental Studies, University of Pretoria article info Sexual selection often involves female preference for males of a certain age, and a body of theory predicts Article history: preference for old males. We measured a comprehensive set of traits from the acoustic sexual display of Received 10 June 2010 male field crickets, Gryllus bimaculatus, and found that nearly all song traits changed predictably as males Initial acceptance 20 July 2010 aged, involving a general slowing down of the wing movements during song production. Our female Final acceptance 9 September 2010 preference experiments indicated a strong and repeatable preference for the songs of young males, Available online xxx contradicting the existing literature, which argues that female crickets prefer older males on the basis of MS. number: 10-00417R changes in song carrier frequency. Rather, female preference for young male song was determined by its high energetic quality. We develop the ‘old flight muscle’ hypothesis, arguing that age-related degradation Keywords: of stridulatory muscle performance is likely to result in the observed changes with age. Secondary sexual calling song characters may be subject to oxidative somatic degradation suggesting that, when males provide only female preference sperm, females should prefer the sexual displays of young males. Our results support new modelling Gryllus bimaculatus senescence approaches and a growing body of empirical evidence suggesting that old males are not always preferred sexual selection by females. Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. The age of a potential mate is an important trait, which can of DNA in the germline is a prominent force in the evolution of mate influence sexual selection. The ‘good genes’ model of sexual selection choice and sexual signalling. If the amount of oxidative DNA damage (Zahavi 1975)predictsthatifthegeneticcharacteristicsrequiredto is correlated with the expression of a secondary sexual character, survive to an old age in the current environment are heritable, then females may avoid the negative heritable consequences by avoiding females should prefer older males as they have demonstrated their sperm damaged by oxidation. The hypothesized mechanism for this viability (Trivers 1972; Halliday 1978, 1983) and are likely to carry is as follows. Oxidation of DNA in the germline takes place with age fewer deleterious alleles (Manning 1985). Modelling approaches through oxidative stress (oxidative stress hypothesis, Sohal et al. attempting to explain the evolution of female preference for males 2002; but see Buffenstein et al. 2008). If the secondary sexual (Hansen & Price 1995; Kokko & Lindström 1996; Kokko 1998; Beck & traits preferred by females are honest indicators of male quality, Powell 2000; Beck et al. 2002; Beck & Promislow 2007), as well as increasing somatic oxidative damage with age will increasingly have empirical studies (reviewed in Brooks & Kemp 2001), have demon- a negative effect on the expression of these traits. In line with the strated different outcomes: female preference may evolve for young, predictions of Beck & Promislow (2007) and Velando et al. (2008), intermediate-aged or old males. It is therefore no longer universally Hoikkala et al. (2008) showed that both reproductive success and accepted that older males always provide good genes. the quality of sexually selected song in Drosophila montana males When females are able to determine a male’sage,preferencefor decrease with male age. Female D. montana are therefore able to younger males is predicted to evolve according to Beck & avoid ‘bad genes’ by preferring younger males on the basis of the Promislow’s(2007)model, assuming an increase in the number of courtship song. deleterious mutations in the germline as a male ages. This model is Because acoustic signals are secondary sexual traits often under of particular relevance in species where females obtain only sperm sexual selection (Andersson 1994) these systems can provide insight from a mating and no other direct benefits: older males are expected into the evolution of female preference. Field crickets (Orthoptera: to be inferior because their fertility is diminished either through Gryllidae) are a particularly well-studied taxon that produce acoustic poor-quality sperm (affecting offspring survival) or insufficient signals by scraping their tegmina (forewings) together. The resulting viable sperm numbers. Velando et al. (2008) proposed that oxidation sound usually has a distinct temporal and spectral structure for each species (Gerhardt & Huber 2002). While certain characteristics of the sound such as the syllable period are thought to be species recog- nition traits (Schildberger et al. 1989; Ferreira & Ferguson 2002), * Correspondence: L. Verburgt, Centre for Environmental Studies, Room 2-1 Geography, University of Pretoria, Pretoria 0001, South Africa. other song traits (e.g. carrier frequency, intersyllable interval, chirp E-mail address: [email protected] (L. Verburgt). rate) are thought to be sexually selected because they are correlated 0003-3472/$38.00 Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2010.09.010 Please cite this article in press as: Verburgt, L., et al., Male field cricket song reflects age, allowing females to prefer young males, Animal Behaviour (2010), doi:10.1016/j.anbehav.2010.09.010 2 L. Verburgt et al. / Animal Behaviour xxx (2010) 1e11 with a male trait (e.g. body size) preferred by females (Simmons & is broad with little preference variation between 4 and 5 kHz (see Ritchie 1996; Gerhardt & Huber 2002; Scheuber et al. 2003a, b; also Verburgt et al. 2008). Therefore, despite the fact that male Jacot et al. 2007; but see Verburgt & Ferguson 2010). For several cricket song does change with age (Table 1), it is unclear whether cricket species it has been shown that certain male song traits females can detect these changes and whether they show a partic- change with age (Table 1), potentially allowing females to select ular directional preference based on these changes. males of preferred age based on song traits. Finally, within the context of the work by Beck & Promislow An interspecies comparison of age-related effects on cricket (2007) and of Velando et al. (2008), it is not clear why female song traits where nutritional condition was not manipulated does crickets should prefer older male crickets, since males of many not reveal a consistent effect on a particular song trait (Table 1). species usually provide only sperm during mating. In Gryllus Moreover, different studies on the same species have found bimaculatus males, reproductive success as measured by progeny contradictory results (e.g. an age-related effect on carrier frequency production per mating decreases significantly with age (Simmons for Gryllus campestris: Simmons 1995; Jacot et al. 2007; Table 1), 1988). Nevertheless, several studies on grylline crickets have usually explained by differences in experimental design. It is demonstrated female preference for older males (e.g. G. veletis and therefore difficult to make generalized predictions of how male age G. pennsylvanicus: Zuk 1987) although no calling song traits in these is expected to affect mating behaviour. species varied with age (Cade & Wyatt 1984; Ciceran et al. 1994). Jacot et al. (2007) used a longitudinal experimental design In acoustic signalling species it is not only the song structure (same animals measured when young and old) to demonstrate that (temporal and spectral traits) that is of importance but also the for male field crickets, G. campestris, age is predictable from the duration (time spent calling) and timing (temporal calling pattern) songs they produce The carrier frequency (frequency of greatest of the song (Walker 1983; Bertram & Johnson 1998; Bertram 2000; power, hereafter FQ), syllable number (syllables per chirp) and Jacot et al. 2008). Old and very young male Gryllus integer spent less chirp length of old males were, on average, lower than for young time calling per night than intermediate-aged males, while old males. Jacot et al. (2007) focused their discussion on the change in males initiated calling earlier in the evening (Bertram 2000). When FQ (nominally 5 kHz), which was, on average, 80 Hz lower for old investigating the effects of age on male song production, it is males, and suggested that females preferentially select older males therefore important to describe changes in the signalling intensity because they prefer lower FQ (Scheuber et al. 2004). However, they and timing thereof. did not experimentally demonstrate that females were able to Our aims in this study were threefold. First, we investigated how detect such a small change in FQ or that the older male song was calling songs change with age by recording male G. bimaculatus preferred. Verburgt & Ferguson (2010) recently challenged the every night for the duration of their adult lives, and by recording current emphasis on song FQ in studies on grylline crickets and a large array of male song traits, thus improving on the longitudinal showed