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Repeat Swimming Performance and Its Implications For 306 Repeat Swimming Performance and Its Implications for Inferring the Relative Fitness of Asexual Hybrid Dace (Pisces: Phoxinus) and Their Sexually Reproducing Parental Species Jonathan A. Mee* which probably contributes to the coexistence of asexual and Colin J. Brauner sexual species in this system. Eric B. Taylor Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada Introduction Accepted 1/23/2011; Electronically Published 3/7/2011 Asexual reproduction is rare among vertebrates; depending on how one defines an asexual “species,” there are only 30–90 known vertebrate examples (Dawley and Bogart 1989; Avise 2008). In contrast with the low number of asexual species, the ABSTRACT theoretical advantages of asexual reproduction are numerous While theories explaining the evolution and maintenance of and have been of interest for well over a century (Darwin 1862; sex are abundant, empirical data on the costs and benefits of Felsenstein 1974; Williams 1975; Barash 1976; Maynard Smith asexual relative to sexual reproduction are less common. Asex- 1978; Charlesworth 1980; Hastings 1999). The most commonly ually reproducing vertebrates, while few, provide a rare op- cited and perhaps the most intuitive and important advantages portunity to measure differences in fitness between asexual and of asexual reproduction include the fact that asexuals pass all sexual species. All known asexually reproducing vertebrates are their genes to their offspring, whereas sexuals pass only half of hybrid origin, and hybrid disadvantage (i.e., reduced hybrid their genes on to their offspring (Charlesworth 1980), and asex- fitness) is thought to facilitate long-term coexistence between ual populations have double the potential growth rate of sexual asexual and sexual species. We used repeat swimming perfor- populations (Lively 1996; Jokela et al. 1997). Based on these mance as a proxy for fitness to compare the fitness of asexual advantages, it is perhaps surprising that asexual reproduction hybrid dace (Pisces: Phoxinus) and their sexually reproducing among vertebrates is not more common. The observation that parental species, finescale dace (Phoxinus neogaeus) and north- asexuality is rare combined with the theoretical expectation that ern redbelly dace (Phoxinus eos). We tested the prediction that, it should be more common has motivated the development of given the widespread coexistence of these hybrid and parental many hypotheses to explain how the advantages of asexual dace, the parental species should show equivalent and perhaps reproduction are balanced or outweighed by advantages in- superior repeat performance relative to hybrids. A repeat con- herent to sexual reproduction (Kondrashov 1993; Agrawal stant acceleration test (Umax) was conducted at both acclimation 2006). Although evolutionary biology is not lacking in theories temperature (16ЊC) and at an elevated temperature (25ЊC) to for why sex is advantageous and common, a thorough under- simulate the combined influence of a repeat swim and acute standing of the reasons why sexual reproduction is common, temperature change that fish might experience in the wild. The particularly among vertebrates, can only be achieved through asexual hybrids performed more poorly than at least one of empirical study of closely related asexual and sexual species. the parental species. There was a negative effect of temperature All known asexual vertebrates have originated from hybrid- on repeat swimming performance in all fish, and the repeat ization (Dawley and Bogart 1989), which may have an impor- performance of hybrids was more severely affected by temper- tant influence on their fitness relative to sexual vertebrates. ature than that of finescale dace. No difference in the effect of Hybrids may suffer disadvantages because of incompatibilities temperature on repeat performance was detected between hy- between the parental species’ genomes, but hybrids may also brids and northern redbelly dace. These results suggest that gain advantages by the creation of novel beneficial genetic var- hybrids suffer physiological costs relative to the parentals or at iants resulting in hybrid vigor. Hybrid vigor might be expected least that the hybrids do not gain advantage from hybrid vigor, to arise spontaneously among asexual vertebrates because of the high degree of genetic heterozygosity characteristic of in- terspecific hybrids (leading, perhaps, to a “general purpose ge- * Corresponding author; e-mail: [email protected]. notype”), or it might be expected to result from interclonal Physiological and Biochemical Zoology 84(3):306–315. 2011. ᭧ 2011 by The selection leading to the persistence of only the most fit hybrid University of Chicago. All rights reserved. 1522-2152/2011/8403-0104$15.00. genotypes (Lynch 1984). There is, in fact, evidence for hybrid DOI: 10.1086/659245 vigor in some asexual vertebrate systems (Hotz et al. 1999; Repeat Swimming Performance of Asexual and Sexual Dace 307 Kearney et al. 2005). In contrast, several theoretical models promelas; Webb 1982), a cyprinid species that co-occurs with have shown that the long-term coexistence of asexual verte- Phoxinus dace across much of its range. Acute exposure to brates with their sexual parental species is facilitated if asexuals temperatures above optimal values, especially when approach- do not gain a fitness benefit from hybrid vigor and especially ing upper lethal temperatures, imposes an additional stressor if the asexuals suffer a fitness loss because of hybrid disadvan- that may reduce swimming performance whether the swim test tage (Moore 1976; Hellriegel and Reyer 2000; Mee and Otto is aerobic or anaerobic in nature (Beamish 1978; Randall and 2010). Hybrid disadvantage has been detected in several asexual Brauner 1991). The ability of a fish to swim fast enough to vertebrate systems (Wetherington et al. 1987; Lively et al. 1990; evade a predator is likely affected by incomplete recovery from Moritz et al. 1991; Weeks 1995; Cullum 1997; Vorburger 2001; a previous evasive swim as well as by temperature, but the Mee and Rowe 2006). It is important to note that these con- influence of an acute temperature change on repeat swimming trasting empirical results (i.e., some asexual vertebrates showing performance has not previously been evaluated. hybrid vigor and some showing hybrid disadvantage) may be The functional morphology and physiology of swimming due to variation in the age of these hybrid asexual lineages. performance is a critical aspect of the life of aquatic animals. Additional data on the ages of asexual vertebrate lineages and In fact, tests of swimming ability have been used for decades on components of fitness of asexual vertebrates and their pa- to test hypotheses concerning the evolution of adaptations of rental species are required for a thorough analysis of the ad- migratory and stream-dwelling fishes (e.g., Brett 1964; Taylor vantages and disadvantages at play in the maintenance of sex and McPhail 1985, 1986; Taylor and Foote 1991; Brauner et al. among vertebrates. 1994; Nelson et al. 2003). Further, tests of repeat swimming Two species of dace (Pisces: Cyprinidae), northern redbelly performance (i.e., when an animal is tested twice in rapid suc- dace (Phoxinus eos Cope, 1861) and finescale dace (Phoxinus cession) have been used to study fish health and the metabolic neogaeus Cope, 1867), have produced asexually reproducing processes involved in recovery from exhaustion (Jain et al. 1998; hybrids that co-occur across much of the parental species’ Jain and Farrell 2003). northern North American ranges. The same clonal hybrid lin- In this study, we used a test of repeat swimming performance eages have probably been coexisting with parental dace pop- to compare the swimming ability, as a proxy for fitness, of ulations across their range ever since the last glacial retreat asexual hybrid dace with that of its sexually reproducing pa- (Angers and Schlosser 2007). Like many asexual vertebrates, rental species. We addressed the effects of multiple stresses, these hybrids are sperm-dependent asexuals and reproduce via namely repeat swimming and increased temperature, on swim- gynogenesis—sperm from a parental species is required for egg ming ability by conducting the repeat swimming performance development but not for its genetic constitution (Goddard et test at both a laboratory acclimation temperature and at an al. 1998). Many hybrid dace populations coexist with only one elevated temperature. We hypothesized that, given the wide- of the two parental species, but several lakes have been shown spread long-term coexistence of these asexual hybrid and sex- to contain both parentals and the hybrid. Even in the lakes ually reproducing parental dace, the asexuals should have hy- with both parental species, there is no evidence that hybridi- brid disadvantage (i.e., reduced fitness relative to the parentals) zation has occurred since the last glacial retreat. Most hybrid or at least should lack hybrid vigor. dace coexist with northern redbelly dace, but a few populations have been found in Alberta and northeastern British Columbia Material and Methods coexisting with only finescale dace (J. A. Mee, personal obser- Study Populations vation). These fishes are an excellent model system in which to evaluate relative fitness as a factor facilitating the coexistence Females from four lakes with populations of hybrid and pa- of asexual and sexual forms because while there is some evi- rental dace were
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