Caring fish dads evolved prostates faster

Caring fish dads evolved prostates faster

Animals caring for their young, such as a lioness carrying her cub by their scruff or a matriarchal elephant herd nursing young calves, are the kinds of behavior that many would pay good money to watch on a safari. However, fish, especially father fish, caring for their young has received limited popular attention, except maybe for the clownfish father-son duo featured in Finding Nemo. Findings published in the recent article “Parental care drives the evolution of male reproductive accessory glands across ray-finned fishes” in the journal Evolution by a group of scientists in Canada shed new light on the evolution of fish paternal care. Lucas Eckert (McGill University), along with his co-advisors Ben Bolker and Sigal Balshine (both at McMaster University) and their co-authors Jessica Miller and John Fitzpatrick, show that, among ray-finned fish, species in which fathers look after young evolved reproductive accessory organs six times faster than those without male care.

Ray-finned fish, bony fish with webbed fins supported by thin, long rays of bone, represent the vast majority of known fish species. Some of these species have reproductive accessory organs, which are parts analogous to prostate glands in humans. These organs are not directly involved in producing gametes, but they optimize reproductive potential through functions such as sperm storage and nourishment. They also produce fluids that increase the ability of sperm to move and fertilize eggs. Research on how these glands evolved has focused mostly on mammals and insects, with little known about their evolution in fish.

“Accessory reproductive glands are a bit of a ‘mystery organ’ when it comes to fish”, says Dr. Sigal Balshine, fish behavioral ecologist and co-principal investigator of this study. “Some fish have them while some don’t have them at all. We know of their existence only in a very few species out of nearly 30,000 fish species in the world. Even when they are present, accessory reproductive glands show bizarre diversity which has always made me think that there must be interesting evolutionary drivers shaping them. There was a lot we didn’t know regarding how or when they evolved, which is why we started collecting data on them”.

In certain groups of animals, sperms of multiple males compete to fertilize the eggs of a single female, a scenario known as sperm competition. Accessory glands produce secretions that enhance sperm performance, and scientists have long believed that they evolved as a weapon to aid in this post-copulatory war in organisms such as rodents and insects. Most fish biologists assumed fish reproductive accessory glands followed the same evolutionary trend. However, in their study, Eckert and colleagues shift the focus away from sperm competition towards parental care. These authors reconstruct the evolutionary history of reproductive accessory organs, testing whether parental care and/or mate competition among males contributed to their evolution.

“There was evidence that these organs were super important in the species that have them, in securing reproductive success and fitness through a variety of functions. In that context, when some species have them and some don’t, the most obvious question was what were the drivers that selected for their evolution in the first place.” says Lucas Eckert, PhD student and lead author of the study, and one of the many students who have been collecting these data since 2017.

The team approaches this question using a quantitative synthesis of phylogenetic, morphological, and behavioral trait data of ray-finned fish collected from published databases. A plethora of published research data is available on reproductive traits of fishes, owing to their remarkable diversity in reproductive organs and behaviors. However, previous studies mostly only describe these traits, without formally testing any hypotheses regarding their evolution. In this study, the authors compile reproductive trait data for over 600 fish species from research conducted over many decades, to quantify the influence that sperm competition and parental care have had in shaping the accessory glands.

In this study, we have been able to put existing data and methods together in ways that they have not been connected before”, says Dr. Ben Bolker, mathematical biologist and co-principal investigator of the study. “This study has been able to find ways to ask the question and find, how much sperm competition and parental care contribute to the evolution of accessory reproductive organs of ray-finned fish, rather than ask what exactly caused accessory glands to evolve, because in biology everything does everything”.

Left: Upside-down round goby (Neogobius melanostomus) male guarding his eggs. Photo by Sina Zarini. Right: Simplified phylogeny highlighting the main ray-finned fish groups in which accessory glands are present (red branches). Illustration by Lucas Eckert.

The special benefits accessory glands provide male fish for improving their reproductive success explains why they evolved faster in species with paternal care. Unlike in many other animal groups where mothers take care of their young, when it comes to fish, that duty was most commonly delegated to fathers by evolution: they had the resources to maximize the survival of fertilized eggs, such as territory, security and nutrition. Accessory glands produce secretions that protect fertilized eggs against microbial infections and increase sperm adhesiveness and the viable period of sperm after release. These secretions allow these stay-at-home fish dads to multi-task in keeping their sperm viable for newly spawning females even while taking care of their young and defending their nests.

Though the evolution of accessory glands is traditionally thought to be driven by sperm competition, this study uncovers a new angle on drivers of fish accessory gland evolution by considering parental care behaviors. The authors hope that these results will encourage researchers to take a closer look at these mysterious glands and consider their potential importance in the species that possess them.

Featured image: Goby eggs by Olivier Dugornay, via Wikimedia Commons (CC BY 4.0).

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