Differential investment in male accessory glands: lessons from a marine fish with alternative reproductive tactics
Male reproductive accessory glands play a number of important roles, including enhancing fertilization success in competitive contexts. Theory predicts that males experiencing greater sperm competition risk (i.e. those adopting the opportunistic tactic) should invest more in accessory glands and ejaculate. However, empirical data show the opposite pattern; males experiencing lower sperm competition risk (i.e. those adopting the conventional guarder tactic) invest more in accessory glands. This pattern has possibly emerged because these organs also function to optimize sperm economy and sometimes also play a role in parental care, which provides more benefits to guarder males. To tease apart these contrasting patterns, we examined tactic-specific investment in and histology of accessory glands, as well as the effect of their fluids on sperm performance in guarder males, using the plainfin midshipman fish (Porichthys notatus). We found that midshipman accessory glands consist of two distinct structures: nodes and lobules, differing in organization and secretory characteristics both between structures and male types. Like other fishes with alternative reproductive tactics, guarder males invested more in accessory glands and in lobules specifically compared to opportunistic sneaker males. Fluids from both lobule and nodes increased sperm velocity in guarder males. Moreover, guarder males increased their investment in accessory glands across the breeding season. Our results suggest that accessory glands may have multiple functions and may even play a role in parental care and olfactory signalling. Our study emphasizes the diversity in form and function of accessory glands and highlights the importance of these organs in reproduction.
We would like to thank Stz’uminius First Nations for their permission to sample at Ladysmith Inlet, and P. Walker and R. Shepherd for granting us access to our field site. We also thank the University of Victoria OAU and Animal Care staff, H. Hicklin and Dr. H. Kreiberg at the Pacific Biological Station in Nanaimo, BC, as well as Dr. F. Juanes, K. Cox, and Dr. J. S. Taylor for logistical support. We are extremely grateful to Drs. A. P. H. Bose, K. M. Cogliati, J. L. Fitzpatrick, and N. Sopinka for their comprehensive field work, as well as to N. Houpt, E. Sadler, T. Warriner, N. Luymes, E. Balke, H. Kou, H. Howe, A. Hassan, A. Mistakidis, Dr. J. Marentette, and Dr. J. Taves for their assistance in the field and with data collection. We thank C. Breggion for aid with histological analyses and Dr. J. L. Fitzpatrick and Dr. T. Pitcher for their many suggestions and guidance on sperm collection and analysis techniques. We would also like to thank Dr. B. Bolker, Dr. J. Dushoff, and the McMaster “data lunch” crew for their SAGE statistical suggestions, as well as S. Gotic for data processing help. We also thank our three anonymous reviewers for their helpful input and suggestions.
This research was supported by grants from the Natural Science and Engineering Research Council of Canada (Grant no. 10538042), the American Museum of Natural History, and from the Department of Psychology, Neuroscience, and Behaviour and the School of Graduate Studies at McMaster University.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no competing interest.
Plainfin midshipman fish are a common intertidal species and their populations are not endangered or threatened. All fish were collected in accordance with permits issued by the Canadian Department of Fisheries and Oceans (scientific licenses XR 50 2010, XR 126 2011, XR 14 2013, XR 121 2014, XR 81 2015, XR 94 2016, and XR 58 2017). All research procedures were approved by the McMaster University Animal Research Ethics Board (AUP’s #10-11-70 and #13-12-52) and the University of Victoria Animal Care Committee (Protocols 2015-009 and 2017-003).
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