Gold Cobra Guppy. Credit: Mark Hanford.
Gold Cobra Guppy. Credit: Mark Hanford.

Placenta Evolution and a Sexual Cold War

With their impressive fins and stunning colours, the poeciliids—a group of small fish that includes guppies, mollies and swordtails—are understandably popular in aquariums. Some have beautiful fan-shaped tails that look like flamenco dresses. Others resemble Kandinsky paintings given life.

But some poeciliids are rare in aquaria, because they are relatively drab—silver-and-black oddities in a family known for extravagance. They also tend to share another weird and less obvious trait: they have placentas.

Unlike most fish, which lay eggs, all poeciliids give birth to live young. Mothers nurture their offspring inside their own bodies. Some produce eggs, but keep them inside their ovaries until the young are ready to enter the world. Others have evolved organs that bring the mother’s tissues so close to her baby’s that she can pass nutrients over—in other words, a placenta. Anatomically, this organ is very different to the placentas that human mothers use to nourish their babies, but it does the same job.

Mammals only evolved placentas once. But the poecilids have evolved these organs on at least eight separate occasions, and in a very short span of time. “The placenta is a very complex organ. Imagine if the eye evolved several times in the hominids. It’s that kind of complexity,” says Bart Pollux from the University of California, Riverside.

Now, Pollux has shown that the rise of the placenta was accompanied by drastic changes in the bodies and lifestyles of the poeciliids. The species with these organs are less ornate. They lack obvious courtship rituals. The males tend to be smaller, but their genitals are bigger. And he thinks that this seemingly unrelated constellation of traits arose because the placenta radically changes the relationship between mothers and their developing young.

Consider an egg-laying species. A female fish loads her eggs with nutritious yolk before they are fertilised. At this point, her investment is set. The most important decision she can now make is to choose a good mate, so her eggs get fertilised by the best possible sperm. In this scenario, the battle of the sexes plays out through discerning females and competitive males. You see bright colours, flashy courtship displays, and perhaps large size differences between the sexes.

In species with placentas, things are different. Mothers continue to provide nutrients to their young long after fertilisation. That opens up a new type of conflict between mother and child. The developing embryo does best if it gets as much nutrition from mum as possible. The mother, however, may do badly at raising future children if she invests too much energy in her current one. So in these species, evolution should drive embryos to want more and mums to hold back.

What about fathers? If the species in question doesn’t form life-long partnerships, a father does best if his mate invests heavily in her current child (which he sired) than in future children (which he won’t). And he can influence her investment because his genes are inside the embryo that’s growing within her. These paternal genes act against her maternal ones in an evolutionary tug-of-war with the baby as the rope.

So, what looks like a conflict between mother and offspring is really still a conflict between male and female. But instead of a showy battle of courtship rituals and bright colours, it’s a covert one that takes place in the womb. It’s a Cold War of the sexes. And that is why the placental species evolve away from showy, flashy traits towards sneaky, understated ones.

Pollux first came across this hypothesis in a paper by David and Jeanne Zeh, published in 2000. “They didn’t know how to test these predictions, but we found a way,” he says. He realised that he needed a large family of animals that have a variety of sexual traits and behaviours, and have evolved placentas over and over again. The poeciliids were perfect.

By studying 110 species, his team showed that the placental ones were less likely to have exaggerated traits like sword tails, wavy fins on their backs, bright colours, or elegant courtship. By contrast, they were more likely to have smaller males and relatively longer genitals. They have moved away from obvious displays that help females to choose mates, and towards traits that make it easier for males to sneak up on females and stealthily mate with them.

The team showed that almost all the poeciliids with placentas have an unusual ability: they can get pregnant while they’re already pregnant. This talent is called superfetation, and it stops any single male from monopolizing an entire litter by fertilising every available egg. Rather than being careful about choosing mates, a female can now mate with many males and let their genes duke it out for investment in the womb.

“It all fit!” says Pollux. All the traits he saw pointed to the same shift from choices and competitions that take place before sex, to subtler battles that are waged after it. Zeh, for one, is pleased to see evidence that supports her hypothesis. “The results of this study fundamentally advance our understanding of sexual selection,” she says.

Of course, this leaves a chicken-and-egg problem. Did the placenta drive the evolution of these other traits, or did the other traits drive the evolution of the placenta? The authors think it’s the former—that’s certainly what the title of the paper implies.

But David Haig from Harvard University, who has studied parent-offspring conflict, thinks it was the other way round. He thinks the first change was a move away from formal courtship and towards forced mating. Now, the males, rather than competing for a female’s attention are competing inside her via their sperm. Haig sees superfetation in the context of this sperm competition, as an adaptation that allows sperm to “get in first” and fertilise eggs before they are fully loaded with yolk. The female continues to add nutritious yolk to what is now an embryo, paving the way for the evolution of a placenta.

Reference: Pollux, Meredith, Springer & Reznick. 2014. The evolution of the placenta drives a shift in sexual selection in livebearing fish. Nature http://dx.doi.org/10.1038/nature13451

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