Multiple male reproductive morphs in the invasive round goby (Apollonia melanostoma)

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Abstract

Alternative male reproductive tactics are taxonomically widespread. In such species, parental, or conventional, males express secondary sexual characteristics, court females and guard offspring, while smaller parasitic or sneaker males avoid the costs of courtship and parental care by performing sneak fertilizations. Theory predicts that sneakers will invest more in testes mass and produce more competitive ejaculates than parentals because sneakers always experience sperm competition while parental males experience sperm competition only when a sneaker is present. Here we present convergent lines of evidence supporting the existence of alternative male reproductive tactics in round gobies (Apollonia melanostoma, formerly Neogobius melanostomus), a recent invader in the Great Lakes. Dark morph males exhibited secondary sexual characteristics, were larger and had higher plasma 11-ketotestosterone concentrations than light morphs, while light morph males invested more in ejaculates (both testes mass and sperm density). Both male morphs had enlarged urogenital papillae, but papillae were relatively longer in light morph males. Sperm tail length did not differ between morphs, and sperm from dark morphs swam faster than sperm from light morphs. Our data strongly argue for the presence of alternative tactics in round gobies, support some predictions from sperm competition theory and align with empirical observations in other taxa. For species of concern like the invasive round goby, it is critical to consider such evidence of alternative male mating tactics when constructing population growth models and assessment of invasion success and impacts.

Introduction

Male alternative reproductive tactics (MARTs) emerge when competition for mating opportunities is fierce and the potential exists for some males to reduce fitness costs by exploiting the reproductive investment of other males (Oliveira et al., 2008). Among fishes, MARTs are particularly common and are taxonomically widespread, because external fertilization is prevalent (allowing simultaneous sperm release from several males), somatic growth is indeterminate (creating large variance in body size and resource sequestering abilities among males), and paternal care is common (providing strong fitness pay-offs to male sneakers that avoid the costs of courtship and parental care; Oliveira, 2006, Taborsky, 1998). The aim of this study was to comprehensively examine the possibility of MARTs in the round goby (Apollonia melanostoma, formerly Neogobius melanostomus), a recent prolific Ponto-Caspian invader of the Laurentian Great Lakes and aquatic biotas in northeastern Europe (Corkum et al., 2004).

Although the round goby poses a serious threat to native fauna ecology and conservation (e.g., Jude et al., 1995), its reproductive habits are still not fully understood. Breeding fish are difficult to observe in the wild (Wickett and Corkum, 1998) and spawning is rarely achieved under laboratory conditions (L.D. Corkum, University of Windsor, personal communication; J.R. Marentette, personal observation), complicating efforts to study reproduction directly. However, understanding round goby reproduction is critically important in terms of predicting the ecological impacts of this invasive species. Round gobies belong to the speciose teleost family Gobiidae that contains several species with male alternative reproductive tactics, including the common goby, Pomatoschistus microps (Magnhagen, 1992), black goby, Gobius niger (Mazzoldi and Rasotto, 2002), and the sand goby, Pomatoschistus minutus (Svensson, 2004). Sneaking behaviour has been observed in the round goby (C. Murphy, University of Alberta, personal communication) and has been reported to occur in a number of publications (Corkum et al., 1998, MacInnis, 1997, Marentette and Corkum, 2008). However, these reports are based on limited laboratory behavioural observations and a few morphological observations.

To investigate the claim of MARTs in round gobies, we examined the external morphology, internal anatomy, endocrinology and sperm characteristics of male round gobies from Lake Ontario in light of sperm competition theory and current knowledge of MARTs in vertebrates. In general, male tactics can be divided into two categories. Parental males, sometimes called conventional, type I or bourgeois males, are large, invest more in growth than in reproduction, defend territories, court females, exhibit secondary sexual characteristics, and have elevated androgen concentrations (Oliveira et al., 2008). In contrast, sneaker, type II or parasitic males are smaller, invest in reproduction at the cost of growth, and lack secondary sexual characteristics. Rather than court females, these sneaker males add their ejaculate surreptitiously to spawnings in progress by stealth, speed, or by imitating females (Oliveira et al., 2008). Males will be subject to asymmetric risks of sperm competition, the competition between sperm from rival males to fertilize a female's ova (Parker, 1970), depending on the reproductive tactic employed. Because parental males are sometimes able to sequester mates and drive off competitors including sneakers, they experience a relatively lower risk of sperm competition. In contrast, sneaker males experience sperm competition during every mating, as by definition they only release sperm in the presence of a parental male. Thus, in order to overcome their disadvantage, sneaker males are expected to invest more in sperm number than parental males (Parker and Ball, 2005). Sperm competition is also thought to lead to sperm with longer flagella that swim faster (Ball and Parker, 1996). Sperm tail length is associated with sperm swimming speed (Fitzpatrick et al., 2009) and, in external fertilizers, sperm swimming speed predicts fertilization success in competitive matings (Gage et al., 2004).

We predicted that if two alternative reproductive tactics exist in round gobies, one morph (presumably the parental male morph) would be larger than the other morph (the sneaker male morph). Since secondary male sexual traits are associated with high levels of androgens, we predicted that plasma concentrations of 11-ketotestosterone (11-KT), the primary fish androgen, would be higher in parental males than in sneaker males (Oliveira et al. 2008). We also predicted that parental males would invest comparatively less in testes mass than sneaker males, and that sneaker males, which encounter higher levels of sperm competition would produce more sperm that have longer flagella and swim faster than the sperm of parental males (Ball and Parker, 1996, Parker and Ball, 2005).

Section snippets

Methods

Round gobies (n = 1295) were collected in minnow traps or by electrofishing from Hamilton Harbour between June 26 to August 23, 2006, and May 16 to August 29, 2007, and from nearby Jordan Harbour in Lake Ontario on July 21, 2006. Traps baited with 25 g frozen corn were set in  <  1 m of water every 2 weeks, and were collected after 24 h. Fish were then transported to McMaster University and maintained in aerated laboratory aquaria before processing.

The sexes were differentiated by the shape of the

External body morphology

Dark morph males were larger (t293 = 19.8, p < 0.0001) and heavier (t293 = 19.3, p < 0.0001, Table 1, Fig. 1a) than light morph males. Dark morph males had wider heads compared with light morphs (ANCOVA, whole model F2,292 = 1865, p < 0.0001; male morph F1,292 = 54.3, p < 0.0001; Fig. 1b).

Gonads and urogenital papillae

Light morph males invested nearly three times as much as dark morphs in testes (median score was 2.8 times more massive; Z =  10.62, p < 0.0001, Fig. 2a), while dark morph males invested twice as much as light morphs in accessory

Discussion

The multiple lines of evidence pursued in this study, including data on external morphology, reproductive investment, endocrinology and sperm characteristics, converge to corroborate the hypothesis that the round goby possesses two morphologically and physiologically distinct male morphs that we predict correspond to alternative male reproductive tactics. The dark morph has traits corresponding to a parental male tactic, and the light morph has traits corresponding to a sneaker male tactic. One

Acknowledgments

The authors would like to thank S. Marsh-Rollo, C. Gross, A. Schermel, A. Stosic, D. Re and K. Gooderham for their help in fish and data collection, L. Corkum for comments on the manuscript and D. deCatanzaro and R. Montgomerie for the use of their facilities. All studies were approved by the McMaster University Animal Research Ethics Board (AREB) and comply with the current laws of Canada (AUPs # 03-09-54 and 06-10-61). This research was supported by the Department of Fisheries and Oceans

References (40)

  • Balázová-L'avrincíkováM. et al.

    Epigenetic context in the life history traits of the round goby, Neogobius melanostomus

  • BurnessG. et al.

    Sperm swimming speed and energetics vary with competition risk in bluegill (Lepomis macrochirus)

    Behav. Ecol. Sociobiol.

    (2004)
  • CorkumL.D.

    Pheromone signaling in conservation

    Aquat. Conserv. Mar. Freshw. Ecosyst.

    (2004)
  • CorkumL.D. et al.

    Reproductive habits of round gobies

    Great Lakes Res. Rev.

    (1998)
  • CorkumL.D. et al.

    The round goby, Neogobius melanostomus, a fish invader on both sides of the Atlantic Ocean

    Biol. Invasions

    (2004)
  • FitzpatrickJ.L. et al.

    Reproductive-tactic-specific variation in sperm swimming speeds in a shell-brooding cichlid

    Biol. Reprod.

    (2007)
  • FitzpatrickJ.L. et al.

    Female promiscuity promotes the evolution of faster sperm in cichlid fishes

    Proc. Nat. Acad. Sci.

    (2009)
  • GageM.J. et al.

    Effects of alternative mating strategies on characteristics of sperm production in the Atlantic salmon (Salmo salar): theoretical and empirical investigations

    Proc. R. Soc. Lond., B Biol. Sci.

    (1995)
  • IguchiK. et al.

    Spawning and brood defense of smallmouth bass under the process of invasion into a novel habitat

    Env. Biol. Fish.

    (2004)
  • JonesA.G. et al.

    Surprising similarity of sneaking rates and genetic mating patterns in two populations of sand goby experiencing disparate sexual selection regimes

    Mol. Ecol.

    (2001)
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