This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Animal Behaviour 78 (2009) 747–753 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/yanbe Potential reproductive rate of a sex-role reversed pipefish over several bouts of mating Sunny K. Scobell*, Adam M. Fudickar 1, Rosemary Knapp 2 Department of Zoology, University of Oklahoma article info The potential reproductive rate (PRR, the rate at which each sex could reproduce if given unlimited Article history: mates) has proven to be a useful tool in predicting the direction and strength of sexual selection. We Received 5 February 2009 conducted a 2-month study of the PRR in the polyandrous gulf pipefish, Syngnathus scovelli, a year-round Initial acceptance 19 March 2009 breeder. In this sex-role reversed species, the female transfers eggs to a male’s brood pouch during Final acceptance 28 May 2009 mating and thus renders him unavailable to mate for 2 weeks. We predicted females would have a higher Published online 4 August 2009 PRR than males and that the rates in both sexes would change over successive breeding bouts in rela- MS. number: A09-00073 tionship to previous reproductive output. Females did have a higher overall PRR than males for the entire study period. However, PRR was not constant across individual breeding bouts. For each sex, the PRRs Keywords: from the first and third bouts of mating were significantly higher than the PRR of second mating bout. gulf pipefish Our results are consistent with individuals making trade-offs between current and future reproductive life-history theory investment. We also discuss how ovarian morphology may contribute to elevated female PRR in this ovarian morphology pipefish species. To our knowledge, this is the first study of PRR in a North American pipefish. potential reproductive rate The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. sex-role reversal sexual selection Syngnathidae Syngnathus scovelli When studying mating behaviour, researchers usually want to However, PI (defined as any effort that increases offspring survival know which sex is under greater sexual selection pressure and to at the expense of the parent’s ability to invest in other offspring) can what degree. This information is useful in determining the sex that be difficult to measure, particularly in species where both sexes should be competitive for mates and the sex that should be choosy. have some form of investment (Clutton-Brock 1991). Emlen & Oring The strength of sexual selection acting on each sex can also be (1977) proposed that a bias in the operational sex ratio (OSR) away correlated with territoriality, the degree of sexual dimorphism and/ from 1:1 could result in an increase in the intensity of sexual or ornamentation and variance in mating success (Andersson selection on the sex that is more abundant. The OSR, which is the 1994). However, measuring the strength of sexual selection acting average ratio of sexually active females to males in a population at on each sex has been difficult historically, and determining which any given time, has been effective in estimating the opportunity for methodology is best has been the subject of debate. sexual selection in several species (Vincent et al. 1994; Kvarnemo & Many researchers have measured sex differences in parental Ahnesjo¨ 1996; Dearborn et al. 2001; Jones et al. 2001). However, investment and/or the operational sex ratio, two indirect measures obtaining an accurate OSR for a population may not be feasible for of the strength of sexual selection. Trivers (1972) proposed that the a particular species being studied and could also vary greatly sex that has relatively greater parental investment (PI) should be temporally (Forsgren et al. 2004), which could in turn have conse- choosy, leaving the sex that has lower PI to compete for mates. quences for conclusions about the strength of sexual selection. In situations where it is not practical to estimate the PI or OSR, the potential reproductive rate can be used to predict the intensity * Correspondence and present address: S. K. Scobell, Department of Biology, of sexual selection. The potential reproductive rate (PRR) is the rate Texas A&M University, 3258 TAMU, College Station, TX 77843-3258, U.S.A. at which each sex in a population could reproduce if given unlim- E-mail address: [email protected] (S.K. Scobell). ited mates (Clutton-Brock & Vincent 1991) and assumes no differ- 1 A. M. Fudickar is now at the Department of Migration and Immuno-ecology, ential immigration or mortality between the sexes (Kokko & Max Planck Institute for Ornithology, Radolfzell, Germany. 2 R. Knapp is at the Department of Zoology, University of Oklahoma, 730 Van Monaghan 2001). The PRR has proven to be a useful tool in pre- Vleet Oval, Room 314, Norman, OK 73019, U.S.A. dicting the direction and strength of sexual selection (fish: 0003-3472/$38.00 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. doi:10.1016/j.anbehav.2009.05.036 Author's personal copy 748 S.K. Scobell et al. / Animal Behaviour 78 (2009) 747–753 Kvarnemo 1994; Kvarnemo & Ahnesjo¨ 1996; Masonjones & Lewis The male fertilizes the eggs and then broods them for about 14 days 2000; Ahnesjo¨ et al. 2001; Wilson 2009; insects: Kvarnemo & (Brown 1972). Thus, male gulf pipefish contribute significantly more Simmons 1998; Wiklund et al.1998; mammals: Preston et al. 2005). time to parental care than do females. The gulf pipefish is also It is usually measured under controlled laboratory conditions sexually dimorphic and has a polyandrous mating system. Females where competition for mates is eliminated and environmental are typically larger than males and have a sexually dimorphic variables are kept constant (i.e. temperature, food, shelter, lack of ornament, a silver bar on each bony ring of the trunk (Reid 1954). predation, etc.). Thus, the PRR controls for many of the confounding Jones et al. (2001) found that mated females in the field had a larger variables that can influence reproductive function and gives an mean snout–vent length, body depth and body mass and were more estimate of the baseline reproductive output for each sex under ornamented than unmated females. They also found that the stan- a similar, constant environment. dardized variance in mating success as measured by microsatellite PRR is typically measured in one of two ways: the number of markers was at least seven times greater in females than in males. offspring (or potential offspring) produced per unit time (Clutton- Despite morphological and genetic evidence supporting Brock & Vincent 1991; Ahnesjo¨ et al. 2001; Wilson 2009) or the a female-biased PRR, it is not known whether male and female gulf ‘time in/time out’ model (Clutton-Brock & Parker 1992). Clutton- pipefish do indeed differ in their respective potential reproductive Brock & Vincent (1991) defined the PRR as the maximum number of rates. If the assumptions underlying sexual selection theory are offspring that each sex produced per unit time. Later, Ahnesjo¨ et al. correct, they should be supported both in species with conven- (2001) measured PRR by counting the number of ‘potential’ tional mating systems and in those that are sex-role reversed offspring produced per day over the course of the breeding season. (Clutton-Brock 2009). The present study was designed to test the They argued that the female’s PRR should be based on the number hypothesis that the sex differences in body size, ornamentation and of eggs released during mating and that the male’s PRR should be parental roles of this species are accompanied by a sex difference in based on the number of eggs fertilized. For the ‘time in/time out’ PRR. The 2-month study period allowed us to measure PRR over model, Clutton-Brock & Parker (1992) defined ‘time out’ as the time multiple breeding bouts. We predicted that females would have period in which an adult is not able to mate, and they defined ‘time a higher PRR than males and that the rates in both sexes would in’ as the time period when an animal is able to mate if given change over successive breeding bouts in relationship to previous a receptive partner. Both methods (‘time in/time out’ and number of reproductive output. offspring/unit time) have proven useful and which method is used often depends on the mating system of the species being studied. METHODS The PRR has been used to study the mating system of several species of syngnathids (pipefish and sea horses). The family Syn- Animals gnathidae is unique among fishes in that male pregnancy is found in all species and some, but not all species, are sex-role reversed We collected sexually mature S. scovelli adults (N ¼ 116) from (Vincent et al. 1992). In species where the PRR of females exceeds sea grass beds in Sarasota Bay, Florida on 6 June 2004. Sexually that of males, the mating system is typically sex-role reversed and mature males have a developed ventral brood pouch and females females compete for access to males. Nerophis ophidion and Syn- have complete silver bars on the trunk (Brown 1972; Jones & Avise gnathus typhle females were estimated to be able to fill the pouch of 1997).