Flexibility in Male Phonotaxis Behavior and the Loss of Singing Ability In
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Behavioral Ecology doi:10.1093/beheco/arp052 Advance Access publication 9 April 2009 Preexisting behavior renders a mutation adaptive: flexibility in male phonotaxis behavior and the loss of singing ability in the field cricket Teleogryllus oceanicus Downloaded from Robin M. Tinghitella, Jeffrey M. Wang, and Marlene Zuk Department of Biology, University of California-Riverside, Riverside, CA 92521, USA http://beheco.oxfordjournals.org/ Flexibility in behavior and other traits can pave the way for rapid evolutionary change. A wing mutation, ‘‘flatwing,’’ eliminates the ability of .90% of male field crickets (Teleogryllus oceanicus) from one Hawaiian population to produce song to attract females. The morphological change was favored because calling is risky in Hawaii, attracting deadly parasitoid flies. An earlier study suggested that instead of calling, silent flatwing males use satellite behavior, approaching one of the few remaining callers and intercepting females attracted to them. Satellite-like behavior may have existed as a behavioral option prior to the wing mutation, accommodating the loss of singing ability, or behavior may have changed simultaneously with the spread of the mutation. In phonotaxis trials, males from different populations across the crickets’ range varied in the distance at which they settled from the source of broadcast song, behaving more or less like satellites. Anecdotally, we noted satellite behavior in all populations, and importantly, males from the mutated population and its direct ancestor behaved similarly. This suggests that the alternative behavior is not strictly associated with the mutation and instead predated the change in morphology. We hypothesized at University of Minnesota,Walter Library Serial Processing on May 28, 2014 further that satellite behavior may have been preexisting because it is beneficial under other circumstances, such as poor mating success. Virgin males did not show enhanced phonotaxis relative to multiply mated males, however. We conclude that satellite behavior predated the mutation in wing morphology, providing obligately silent males with an alternative method of locating mates and effectively rendering the wing mutation adaptive. Whereas mating history does not appear to influence phonotaxis behavior in males, other factors such as the acoustic environment and demographic conditions may be important contributors to behavioral decisions during male mate location. Key words: alternative mating behavior, flatwing, phonotaxis, rapid evolution, satellite. [Behav Ecol 20:722–728 (2009)] exual signals are critical for mate location and courtship, otherwise be maladaptive (Baldwin 1896; West-Eberhard 2003; Sbut intraspecific variation in mating signals and behavior Ghalambor et al. 2007). is pervasive (Darwin 1871; Andersson 1994; Shuster and Wade Field crickets display one commonly investigated example of 2003). For instance, males frequently use alternative mating alternative mating behaviors in which both genetic and envi- behaviors such as female mimicry, satellite behavior, or ronmental components likely play a role. Typically, males ‘‘sneaky mating’’ to attract mates, and these behaviors are are stationary and produce long-distance songs to attract loco- often associated with distinct morphologies (Gross 1996; motory females from afar (Alexander 1961). Rather than call- Shuster and Wade 2003). Alternative mating behaviors can ing, however, some males act as satellites, silently intercepting be genetically distinct, such that a given male can only use females who have been attracted to the call of another male one (sometimes called strategies), or all males can be genet- (Cade 1975; Hissmann 1990; Zuk et al. 1993). Satellite behav- ically monomorphic but utilize one behavior in favor of an- ior exists as an alternative for numerous insects and anurans other under certain conditions, in particular environments, or (Gross 1996; Shuster and Wade 2003). Cade (1981a) selected when their status changes (sometimes called tactics) (Gross for calling and silent behavior in male Gryllus integer 1996). It has been argued, however, that such a dichotomy and found singing behavior to be about 50% heritable. In likely oversimplifies the situation, and many of our examples G. integer (as well as other field crickets), calling males attract may actually be from a fairly continuous distribution of mat- phonotactic parasitoid flies, which may in part explain why ing behaviors (Andersson 1994; Shuster and Wade 2003). Plas- not all males call (Cade 1979; Zuk et al. 1993). Males may ticity in behavior and other traits can pave the way for rapid switch from calling behavior to silent satellite behavior even evolutionary change by allowing a trait to be favored that may within a night (Rowell and Cade 1993; Hack 1998), and sat- ellite behavior may be preferred because it is less energetically expensive than calling (Hack 1998) or simply because an individual has experienced little success as a caller. Address correspondence to R.M. Tinghitella, who is now at Kellogg Both female and male field crickets will approach the calling Biological Station, Michigan State University, 3700 East Gull Lake song of conspecifics (Pollack 1982; Kiflawi and Gray 2000). Drive, Hickory Corners, MI 49060, USA. E-mail: [email protected]. Normally, however, males settle some distance from other sig- J.M. Wang is now at the University of California San Francisco School of Dentistry, 707 Parnassus Avenue, D4010 San Francisco, CA 94143, naling individuals. For instance, the Polynesian field cricket, USA. Teleogryllus oceanicus, has a nearest neighbor distance of at least Received 10 July 2008; revised 3 March 2009; accepted 5 1 m (Zuk M, unpublished data) similar to that found for March 2009. G. integer (Cade 1981b). Male phonotaxis may function in hab- itat selection, territorial spacing, or the formation of mating Ó The Author 2009. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: [email protected] Tinghitella et al. • Preexisting behavior renders mutation adaptive 723 aggregations (Ulagaraj and Walker 1973; Cade 1979; Campbell microhabitat. Males who have not experienced mating success and Shipp 1979). When males behave as satellites, however, as callers might do better by making the ‘‘best of a bad job’’ as they show enhanced phonotaxis, coming into extremely a satellite (Eberhard 1982). A simple decision rule such as close contact with the signaling male, rather than settling ‘‘move toward conspecific song when not mated recently’’ some distance away (Cade 1980). Empirical and theoretical could move an individual into an area of higher local popu- work suggests that satellite behavior can be as successful as lation density where mating may be more common. We sug- calling (Alexander 1961; Hissmann 1990, 1991; Cade WH and gest that mating experience may be important in this system Cade SE 1992; Rowell and Cade 1993; Walker and Cade 2003). also because there is a precedent for phonotactic responses of The flexible expression of alternative mating behaviors has females to depend on recent mating success. In multiple the potential to facilitate evolutionary change by creating an cricket species, female phonotaxis behavior is affected by environment in which ordinarily maladaptive genetic changes mating history, with virgin females having enhanced levels can spread (Baldwin 1896; West-Eberhard 1989, 2003; Yeh and of phonotaxis (measured as distance traveled to a broadcast Downloaded from Price 2004; Ghalambor et al. 2007). Examples in which phe- song, speed of response, or response vs. no response) relative notypic plasticity has facilitated rapid evolutionary change in to singly or multiply mated females (Koudele et al. 1987; sexually selected traits seem to be rare. For instance, Yeh and Loher et al. 1993; Prosser et al. 1997; Lickman et al. 1998). This colleagues documented a rapid reduction in the white color may be the case for males as well. of the tails of dark-eyed Juncos after their introduction to the Here, we investigate variation in male phonotaxis behavior University of California, San Diego campus (Yeh 2004; Yeh in 4 populations of T. oceanicus. We asked 2 questions. First, http://beheco.oxfordjournals.org/ and Price 2004). The change in morphology was possible did satellite behavior predate the mutation to flatwings, pro- because plasticity in breeding season length allowed some viding obligately silent males with an alternative mode of mate females to begin breeding earlier, which aided population location? And second, regardless of wing morphology, is the growth during the early stages of invasion in an environment switch to this alternative mate-searching mode influenced by that favored lesser white color in the tail (Yeh and Price 2004). mating history? Satellite behavior may either have already ex- Here, we investigate an example in which satellite behavior isted as a behavioral option in the crickets’ repertoire (predat- may have facilitated the spread of a mutation that eliminated ing the change to flatwing morphology and rendering the singing ability in a Hawaiian population of Polynesian field wing mutation adaptive) or a series of behavioral changes crickets (T. oceanicus). A recent single-gene mutation that may have taken place simultaneously with the change in wing eliminates the calling structures on the forewings of males morphology. If variation in male phonotaxis behavior preda-