Water Ph During Early Development Influences Sex Ratio and Male
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Zoology 116 (2013) 139–143 Contents lists available at SciVerse ScienceDirect Zoology journa l homepage: www.elsevier.com/locate/zool Water pH during early development influences sex ratio and male morph in a West African cichlid fish, Pelvicachromis pulcher ∗ Adam R. Reddon , Peter L. Hurd Department of Psychology, University of Alberta, Edmonton, Alberta, Canada a r t i c l e i n f o a b s t r a c t Article history: Environmental sex determination (ESD) is one of the most striking examples of phenotypic plasticity. Indi- Received 27 June 2012 viduals from species that exhibit ESD can develop as either males or females depending on the particular Received in revised form 31 October 2012 environmental conditions they experience during early development. In fish, ESD species often show a Accepted 22 November 2012 relatively subtle effect of environment, resulting in a substantial number of both sexes being produced in Available online 7 March 2013 both male- and female-biasing conditions, rather than the unisex clutches that are typical of many rep- tiles. This less dramatic form of ESD allows the opportunity to study the effects of sexual differentiation Keywords: on within-sex variation in behavior and morphology by comparing same-sex individuals produced in Pelvicachromis pulcher male- and female-biasing conditions. Here, we confirm that sex determination in the West African cich- Environmental sex determination lid, Pelvicachromis pulcher, is influenced by pH during early development. We show that pH also affects Phenotypic plasticity pH treatment the ratio of two alternative male reproductive types with the polygynous morph being overproduced in Aggression male-biasing conditions and the monogamous male morph being overproduced in female-biasing condi- tions. Our results suggest that the sexual differentiation process may be an important force in maintaining individual variation in behavior and reproductive tactics. © 2013 Elsevier GmbH. All rights reserved. 1. Introduction often strongly deterministic and small changes in the environment can lead to single-sex clutches (Bull and Vogt, 1979; Janzen and Phenotypic plasticity is the ability for a given genotype to gener- Paukstis, 1991). In fish, however, ESD is typically subtler, and a sub- ate alternative phenotypes depending on the environment in which stantial number of the minority sex are normally produced (Römer that phenotype is expressed (Schlichting, 1986; West-Eberhard, and Beisenherz, 1996; Devlin and Nagahama, 2002). This more 1989; Thompson, 1991). Phenotypic plasticity is adaptive in vari- restricted form of ESD in which the sex of the developing animal is able environments in that it allows the phenotype to be matched to influenced, but not completely determined, by the ambient envi- the ambient environmental conditions, permitting greater flexibil- ronment allows the unique opportunity to investigate within-sex ity in the face of environmental uncertainty (Pigliucci, 1996, 2001, effects of phenotypic plasticity. The sexual differentiation process, 2005; Dingemanse et al., 2009). guided by the developmental environment, may generate differ- Environmentally influenced sex determination (ESD) is the pro- ences between the phenotypes of same-sex animals produced in cess by which the sex of a developing animal is influenced or different environments (Crews et al., 1998; Rhen and Crews, 2002; determined by the environmental conditions in which that animal Crews and Groothuis, 2005). For example, females that develop as develops (Bull and Vogt, 1979; Kraak and Pen, 2002). ESD repre- the minority product of male-biasing conditions may show more sents one of the most striking examples of phenotypic plasticity in male-typical morphology, physiology and/or behavior (Rhen and that a single genotype can produce either male or female phen- Crews, 2002). Conversely, males produced as the minority product otypes depending on the environmental conditions experienced of female-biasing conditions may exhibit a greater preponderance during development (Kraak and Pen, 2002). Among vertebrates, of female-typical characteristics. These subtle effects of the sex ESD has been observed in both fish and reptiles (Janzen and determination and differentiation process may be an important Paukstis, 1991; Devlin and Nagahama, 2002). In reptiles, ESD is source of phenotypic variation (Crews and Groothuis, 2005). Pelvicachromis pulcher is a species of small cichlid fish found in rivers and streams in West Africa (Heiligenberg, 1965; Nwadiaro, 1985). P. pulcher are biparental substrate spawners which exhibit ∗ Corresponding author. Present address: Department of Psychology, Neuro- long periods of parental care (Nelson and Elwood, 1997). P. science and Behaviour, McMaster University, 1280 Main Street West, Hamilton, pulcher males exist in two morphs defined by the color of Ontario, Canada L8S4L8. Tel.: +1 905 525 9140x26037; fax: +1 905 529 6225. their opercula (Heiligenberg, 1965; Fig. S1 in the supplementary E-mail addresses: [email protected], [email protected] (A.R. Reddon). online, Appendix). Yellow opercula males (YO) are monogamous, 0944-2006/$ – see front matter © 2013 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.zool.2012.11.001 140 A.R. Reddon, P.L. Hurd / Zoology 116 (2013) 139–143 engaging in a single reproductive bout with a single female at any with several artificial plants, flowerpots and lengths of black PVC given time. Red opercula males (RO) are facultatively polygynous pipe to serve as potential nest sites. Fish were fed daily on dried and and may breed monogamously or hold a harem of two or more frozen prepared cichlid foods and water temperature was main- ◦ females simultaneously, each of which maintain their own sub- tained at 26 ± 2 C for the duration of the study. Water in the stock territories within the RO’s territory (Martin and Taborsky, 1997; aquaria and in the breeding aquaria before and after our manipula- Barlow, 2000). YO males may also act as satellites on polygynous tions was held at pH 6.0 ± 0.1. These pH and temperature conditions RO males’ territories (Martin and Taborsky, 1997). P. pulcher also mimicked the natural habitat of this species (Nwadiaro, 1985). show a conspicuous sexual dimorphism at sexual maturity with the After 48 h acclimation time in the breeding tanks, we began the females being shorter and deeper bodied with brighter coloration pH treatments. We randomly selected 4 of the 8 breeding aquaria than the males which are more streamlined and less colorful (Fig. S2 and gradually lowered the pH to 5.5 ± 0.1 and in other 4 breeding in the supplementary online, Appendix). Female coloration varies aquaria we gradually raised the pH to 6.5 ± 0.1. We based these continuously between individuals, but females do not show distinct treatments on the previous study reporting pH-dependent ESD in morphs. It has been assumed that the male morphs are genetically P. pulcher (Rubin, 1985) and on the range of pH values measured in determined and fixed throughout life (Heiligenberg, 1965), though their native habitat (Nwadiaro, 1985). We chose to manipulate pH evidence for this claim is scarce. We know of no data as to the rel- prior to spawning in order to completely standardize the exposure ative frequency of the RO and YO morphs in the wild, though both of the offspring to their pH conditions and ensure offspring were subtypes are present (Martin and Taborsky, 1997). exposed to their treatments as soon as the eggs were laid. We main- An earlier paper reported that P. pulcher show ESD dependent on tained our experimental pH using commercially available aquarium water pH during development, with more acidic conditions produc- pH buffer (Seachem Laboratories, Madison, GA, USA) and we mon- ing a greater proportion of males than do more neutral conditions itored the pH in our experimental aquaria daily using a portable (Rubin, 1985). As with other instances of ESD in fishes (e.g., Römer electronic pH meter (pHep 4; Hanna Instruments, Woonsocket, RI, and Beisenherz, 1996), the environmental influence on sex is not USA). absolute in P. pulcher and substantial numbers of the opposite sex The parent fish lived and bred within their experimental pH con- are produced in sex-biasing pH conditions, allowing us to compare ditions. We conducted weekly water changes of 10 l using water males and females from each developmental condition. that had been pre-buffered to match the pH treatment condition. The goals of the current study were threefold. First, we wanted We checked the breeding aquaria daily for the presence of eggs to replicate a previous study (Rubin, 1985) and confirm that sex and all pairs spawned within 21 days of the onset of treatment. is indeed influenced by developmental pH in P. pulcher. Second, We maintained the pH treatments for 30 days after the pair had we wanted to determine whether pH conditions influenced the spawned, after which we allowed the aquaria to gradually return expression of alternative male morphs, specifically, the ratio of to the standard pH (6.0) maintained in our laboratory. We allowed RO to YO males, in an effort to determine whether male morph the parents to remain with their offspring and provide parental care is genetically determined as previously suggested, or if this aspect until 60 days post-hatching, at which point we removed the parents of the P. pulcher phenotype is also plastic and influenced by the and returned them to the stock aquaria. Following the removal of same developmental conditions that influence sex. If RO males the parents, we split each clutch into two separate 110 l aquaria to represent a more masculinized male form, it is conceivable that reduce density and speed maturation. Mortality was monitored and male-producing pH conditions will also produce a higher propor- was rare. The vast majority of the F1 generation survived into adult- tion of the RO type than do female-biasing pH conditions. Finally, hood, and there was no indication of differential mortality between we wanted to determine whether developmental pH affected indi- the treatment groups.