The Laws of Attraction: Mangrove Killifish Style

In the game of love, we typically think of males as being the showy courting sex and females being the coy choosy sex. But what if your species doesn't have the simple division of males and females?

Most populations of animal species (and most notably our own) are roughly half male and half female, so this is the standard we tend to accept as "normal". In this common system, males generally invest less in each potential offspring than do females (in physical resources, parental time and risk), so they can afford to make a few poor mate choices in favor of having more mates over time. Females, on the other hand, have a lot more to lose and benefit from being picky about whom they chose to mate with. But this half-male/half-female system is not the only way to divide reproductive responsibilities... And how these responsibilities are divided can dramatically affect who is choosing whom.

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The mangrove killifish (Kryptolebias marmoratus) is one such species. Most mangrove killifish are hermaphrodites (individuals with both functional male and female sex organs) that possess the ability to reproduce with themselves (a process, amusingly enough, called selfing). This puts a whole new twist on the mate choice problem: If you can reproduce with yourself, who needs a mate at all? In fact, despite the fact that these hermaphroditic fish have both male and female parts, they don't seem to ever mate with one another. But some mangrove killifish (somewhere between 2-25%, depending on the population) are males. There are no female mangrove killifish. So in this system, males can only mate with hermaphrodites. Hermaphrodites can mate with males or with themselves, but not with other hermaphrodites. Got it?

Researchers Amy Ellison, Jennifer Jones, Charlotte Inchley, and Sofia Consuegra at Aberystwyth University in the United Kingdom, recently explored how this hermaphrodite/male reproductive system could impact the mate choice decision making process. They figured that mangrove killifish (like just about any species) would benefit from having more genetic diversity in the population and that individual killifish that are less inbred would be healthier. Therefore, hermaphrodites should choose mating with a male over mating with themselves and both sexes should choose mates that are as genetically different from themselves as possible.

The researchers tested mangrove killifish from two different genetic lines. First, they tested hermaphrodites in a tank in which the fish could choose to hang out with a male or with another hermaphrodite. They much preferred the company of the male (as the researchers had suspected they would). Then they put the hermaphrodites in a tank in which they could choose to hang out with a closely-related male or a distantly-related male. The hermaphrodites didn't seem to care: Apparently any male is good enough.

Then the researchers repeated the study to see what the males preferred. First, they tested males in a tank in which the fish could choose to hang out with a hermaphrodite or with another male. Surprisingly, the males spent as much time with other males as they did with hermaphrodites... But this was apparently because physically challenging a male is as fun as courting a hermaphrodite. When the researchers put the males in a tank in which they could choose to hang out with a closely-related hermaphrodite or a distantly-related hermaphrodite, they much preferred the distantly-related hermaphrodite.

It's hard to find a mate when you live in this environment... especially if potential mates are rare.

So both males and hermaphrodites are choosy about whom they mate with... to a degree. Hermaphrodites seem to prefer to mate with males, but which male doesn't matter. Males, on the other hand, prefer to mate with distantly-related hermaphrodites (when not challenging other males). This system actually makes a lot of evolutionary sense when you consider the ecology of the species. Mangrove killifish populations are mostly hermaphrodites with only small percentages of males. If males are only rarely encountered, a hermaphrodite would benefit from mating with it rather than waiting to see if another better male comes around. (In fact, species that rarely encounter the opposite sex are less likely to develop strong mate preferences compared to species that regularly encounter many individuals of the opposite sex at the same time). Males, however, more frequently encounter hermaphrodites and can afford to wait for the ones that are more distantly related and would have healthier babies.

In the end, it's not what sex you are that makes you choosy or flirtatious. It's what you are risking, what you have to gain, and what your options are that matter.

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Further reading:
Ellison, A., Jones, J., Inchley, C., and Consuegra, S. Choosy males could help explain androdioecy in a selfing fish, The American Naturalist, 181:6, 855-862 (2013). DOI: 10.1086/670304.

Image Credits:
Mangrove rivulus by D. Scott Taylor at Wikimedia Commons.

Mangroves by the US National Oceanic and Atmospheric Administration Wikimedia Commons.