Sneaky males attempt to fertilize fish couples’ eggs in passing

But female fish protect their eggs from the sperm of interlopers with ovarian fluid.

Some ocellated wrasse are stand-up guys. They build cozy algae nests and stick around to help care for their young. It’s no wonder these nest-building, child-rearing fellows are preferred mates for females, who deposit their eggs in males’ nests to be externally fertilized. But not all males are so stable and respectable. Another group of “sneaker males” employs a different reproductive strategy: they swim by and release sperm into the nests of other males as they mate. Fortunately, a recent Nature study reveals that females have some tricks up their sleeves to ensure that their eggs are fertilized by the right guy. Evolutionary biologist Suzanne Alonzo tells us more.

ResearchGate: What are “sneaker males” in ocellated wrasse populations?

Suzanne Alonzo: There are three male types. Nesting males build nests out of algae, court females and take care of the young. Sneaker males don't build nests, court females or take care of their own offspring. Instead, they swim into the nest when a female and nesting male are reproducing and release sperm. Nesting males are large and colorful, while sneakers are small and not colorful. The third type of male are called satellites, which are intermediate in size and color. They don't build nests or care for the young, but they help nesting males chase sneakers away from the nest.

There are many species that have territorial and non-territorial males, and these “alternative male types” as they are called can be found not just in fish but also insects, birds, mammals and beyond. Satellite males are found in a few species, but are much less common.

RG: Why is there such variety in male behavior?

Alonzo: Presumably all three types of males exists because they represent three different ways of achieving reproductive success.  We know sneakers are both younger and slower-growing than males that end up as nesting males. Sneakers may therefore exist because they are a way of achieving reproductive success even if you can't grow large enough, fast enough to succeed at being a nesting male.

RG: How do females control which sperm fertilizes their eggs?

Alonzo: Females produce an ovarian fluid, which they release with the egg. This increases how quickly and accurately sperm move towards the egg, giving an advantage to faster sperm. Nesting males produce less sperm than sneaker males, but their sperm is generally faster. Thus, the ovarian fluid gives them an advantage in the “race" to fertilize the egg.

RG: Why do the two types of males have such differing sperm characteristics?

Alonzo: While I could hypothesize, so far we don't know exactly why they differ. This paper shows for the first time that they differ at all in this species. In other species, researchers have actually found that sneaker males have faster sperm, but we found the opposite here.

RG: What is the significance of your findings for how we understand animal reproduction more broadly?

Alonzo: In species with internal fertilization, we have known for at least a decade that females can influence who fathers their offspring, even after mating. But now we know females can also affect which type of male fertilizes her eggs even when fertilization happens outside the body. This means females also influence which male traits are favored or not favored evolutionarily. This opens up a whole realm of new possibilities—not just for new research but also for thinking about what drives the patterns we see in the marine and freshwater environments. Which adult male traits evolve in terms of courtship or parental care might depend on cryptic interactions happening not between adult males and females, but rather between egg and sperm in the water.

Featured image: A nesting male with a female in his nest. Credit: Susan Marsh-Rollo