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Female Alpine Newts (Triturus Alpestris) Mate Initially with Males Signalling Fertility Benefits

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Female Alpine Newts (Triturus Alpestris) Mate Initially with Males Signalling Fertility Benefits Blackwell Publishing LtdOxford, UKBIJBiological Journal of the Linnean Society0024-40662007 The Linnean Society of London? 2007 91? 483491 Original Article ALPINE NEWT FEMALE CHOICE FOR SIGNS OF FERTILITY P. E. A. HOECK and T. W. J. GARNER Biological Journal of the Linnean Society, 2007, 91, 483–491. With 2 figures Female alpine newts (Triturus alpestris) mate initially with males signalling fertility benefits PAQUITA E. A. HOECK and TRENTON W. J. GARNER* Zoologisches Institut, Universität Zürich, Winterthurerstrasse 190, 8057, Zürich, Switzerland Received 24 March 2006; accepted for publication 1 September 2006 Gametic asymmetry implies that females invest more per gamete than males do and thus sperm is considered to be a relatively cheap resource. However, contrary to this classic view, sperm has been shown to be frequently in short supply; hence, selection favouring females that mate for fertility benefits should occur. For this reason, we determined whether males signalling fertility are preferred by female newts of the species Triturus alpestris. We performed paired female–male trials using unmated and previously inseminated females to determine potential criteria for female interest in a courting male, to establish what factors lead to successful mating and to assess the importance of female choice for direct and indirect benefits. We found that female interest in any potential mate and mating success decreased once mating had occurred. Furthermore, we detected an increase in spermatophore dep- osition rate and rapid spermatophore transfer in encounters that resulted in a successful mating. The results obtained indicate that female alpine newts are attracted to males showing signs of relatively high fertility and that females exhibit a decreased propensity to mate once initial sperm reserves have been acquired. Our results support the theory of initial female choice for fertility benefits. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 483–491. ADDITIONAL KEYWORDS: amphibian – mate preference – sexual selection. INTRODUCTION Phillippi & Yund, 2001; Garcia-Gonzalez, 2004). The- ory thus predicts that limited reserves and circum- A classic view of the sexes is that females are frugal spect sperm allocation should select for female choice with their gametes but males take advantage of their for fertility benefits (Wedell et al., 2002; Parker, 1970). relatively unrestricted supply of sperm to inseminate For internally fertilizing species, polyandry is the as many females as possible (Trivers, 1972). Although most common example of female choice for fertility gametic asymmetry in terms of both size and number benefits. When the operational sex ratio is female- are facts, sperm are actually costly to produce and a biased and individual males lack sufficient resources limited resource (Dewsbury, 1982; Wedell, Gage & for continuous effective insemination, both fecundity Parker, 2002; Montrose, Harris & Moore, 2004). and fertility may suffer; effects that can be alleviated Demography, male physiology, polyspermy, sperm by female remating (Pitnick, 1993). Similarly, male competition, and female choice all impose demands on sperm quality varies enormously, to the point where a male’s ability to produce sperm and how many some males exhibit complete infertility due to sterility. should be allocated to a given ejaculate (Wedell et al., By mating with multiple males, females can compen- 2002; Ball & Parker, 2000). Sperm are therefore fre- sate for any one sterile male, or even for a series of rel- quently in short supply and females are often exposed atively infertile males (Sheldon, 1994; Singh, Singh & to environments where their gametes are at risk due Hoenigsberg, 2002; Garcia-Gonzalez, 2004). Sperm to the unavailability of fertile sperm (Stewart-Savage, usage may be inefficient, and large numbers of sperm are sometimes required to fertilize a single ovum (Török et al., 2003). In species with large clutch sizes *Corresponding author. Current address: Institute of Zoology, Zoological Society of London, Regent’s Park NW1 4RY, London, and/or a prolonged breeding season, polyandry may be UK. E-mail: [email protected] an ongoing requirement for no other reason than © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 483–491 483 484 P. E. A. HOECK and T. W. J. GARNER fertility demands (Jones, Adams & Arnold, 2002; Vie- choice for indirect compatibility benefits may not ites et al., 2004). It is perhaps for these reasons that describe the entire spectrum of female preferences for female choice for benefits directly affecting fertility this species. Males become more circumspect with and fecundity are as important, if not more so, than regards to spermatophore production and the success choice for indirect benefits (Møller & Jennions, 2001), rate of spermatophore transfer for the entire genus is and at least a major factor as to why polyandry is so on the order of one in four under ideal laboratory con- predominant (Garcia-Gonzalez, 2004). ditions: rates are probably poorer in the field (Halli- However, female choice strictly for fertility benefits day, 1990). Although the operational sex ratio favours is not the rule because, in the majority of cases, a male excess at most locations and early in the breed- females are balancing choice for several requirements ing season, female excesses do occur and can reach the and attempting to overcome paternity control mecha- level of two females for every male (Schnüriger, 2004). nisms used by competing males (Eberhard, 1996; Population densities may reach levels as high as 58 Gavrilets, 2000; Martin & Hosken, 2003). Variation in individuals per square meter of pond substrate but, in the demographic and genetic characteristics of the some cases, density is low enough (three per square breeding assemblage and an unpredictable insemina- meter) to negatively influence the encounter rate tion status of individual females can lead to the (Schnüriger, 2004). These demographic and behav- evolution and maintenance of multiple female prefer- ioural patterns suggest that females should encounter ences (Iwasa & Pomiankowski, 1994; Johnstone, 1995, sperm-limited situations and, in these circumstances, 1996; Pitcher et al., 2003; Mays & Hill, 2004) with the exhibit a preference for males signalling fertility ben- result that female choice can become plastic (Qvarn- efits rather than genetic compatibility benefits. strom, 2001; Mays & Hill, 2004), or may exhibit shifts The present study aimed to determine if fertility in preferences based on requirements for direct and benefits are sought by female T. alpestris. We per- indirect benefits (Gabor & Halliday, 1997; Pitcher formed paired female–male trials using naïve and et al., 2003). Even so, when fertility assurance is the experienced females to determine potential criteria for dominant force behind female choice, female promis- female interest in a courting male, to establish what cuity is evolutionarily stable and any choice for indi- factors lead to insemination, and therefore to assess rect benefits should occur postcopulation (Fishman, the importance of female choice for direct and indirect Stone & Lotem, 2003). benefits. We set male courtship vigour and body size as In amphibians, polyandry has been detected in both fitness-correlated phenotypic traits to test for female externally and internally fertilizing species (D’Orgeix choice for good genes and determined overall genetic & Turner, 1995; Laurila & Seppä, 1998; Byrne & Rob- similarity between mating partners post hoc to test for erts, 1999; Osikowski & Rafinski, 2001; Jones et al., female choice for genetic compatibility. Specifically, we 2002; Garner & Schmidt, 2003; Lodé & Lesbarrères, asked the following questions: 2004; Vieites et al., 2004) and fertility benefits have 1. Do female insemination status, male courtship been described for both fertilization strategies experience, vigour, body size, and/or genetic compo- (Osikowski & Rafinski, 2001; Jones et al., 2002; Vie- sition affect a female’s interest in a male and her ites et al., 2004), but not in all cases (Byrne & Roberts, decision to accept or reject him as a potential mat- 1999, 2000). Female choice has been implicated in ing partner? numerous amphibian mating systems, primarily in 2. Do female insemination status, male courtship the context of Fisherian processes (Halliday & Tejedo, experience, vigour, body size, and/or genetic compo- 1995; Sullivan, Ryan & Verrell, 1995; Welch, Seml- sition distinguish successful mating trials (insemi- itsch & Gerhardt, 1998), but evidence for sperm limi- nation of the female) from unsuccessful ones? tation (Osikowski & Rafinski, 2001; Jones et al., 2002; Vieites et al., 2004) suggests that female choice should MATERIAL AND METHODS not be limited to indirect benefits. In a study investi- gating the potential for multiple female preferences in Adult T. alpestris were collected on land from pit fall caudates, Gabor & Halliday (1997) showed that, until traps while migrating to their native pond near mated once, female smooth newts lack discrimination Adlikon, Kanton Zürich, Switzerland (47°35′N, for male traits signalling Fisherian quality. They 8°42′E) at the beginning of March 2001. Capture on interpreted the observed pattern as a trade-up to bet- land ensured that the females were unmated that year ter quality males once fertility had been assured before the start of the experiment (Pecio, 1992). Ani- (Gabor & Halliday, 1997). mals were
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