Will male cottony cushion scales survive their own mating strategy?

Cottony cushion scale hermaphrodite surrounded by her offspring.

A friend of mine just brought my attention to this article in the New York Times Science section today. An insect known as the cottony cushion scale (Icerya purchasi) exists in two sexes: hermaphrodites and males.

Here’s the twist: the hermaphrodites are females infected with the parasitic tissue of a male (her “father”). This parasitic tissue is able to act as the male part of the insect and all0ws her to fertilize her own eggs. So, if the hermaphrodites can just fertilize their own eggs, what do they need the males for?

At first, this sneaky strategy of infecting the females to make hermaphrodites was a pretty smart idea for the males: they are guaranteed to fertilize the eggs of the infected female, thereby passing on their genes to a large number of offspring. In doing this, however, they may have doomed the male sex to extinction. According to new research based on mathematical models of the cottony cushion scale’s populations, the parasitic infection may benefit both males and females. This spells trouble for the continued existence of male individuals.

Hermaphrodites (individuals that are both male and female) are not rare in the animal kingdom, but they are very rare among insects. If you exclude insects, then 30% of animal species are hermaphroditic. Only three insect species, all of which are scale insects, are hermaphrodites. One of these is the cottony cushion scale, Icerya purchasiNobody knows why there aren’t more hermaphrodite insects.

But the hermaphroditic cottony cushion scales are really, really weird. The hermaphrodites have ovitestes (a gonad that makes eggs and sperm)–just like you would expect–but the testes part is haploid while the rest of the animal is diploid. What else are haploid? Sperm. Based on other research on this species, it looks like the testes were actually produced when extra sperm penetrated the egg at the time the female was conceived. The sperm somehow then developed into a haploid tissue that could produce more sperm.

Why would this be good for a male? First, the male can now fertilize the eggs of his daughter, his granddaughter, and so on. Therefore, he’ll have many more mates than he would have otherwise, even after he’s dead. That’s less work for him. The other nice thing about this for the males is that the female (now a hermaphrodite) will produce only hermaphrodites. That way, the male genes get passed onto each and every child. Normally in these insects, fertilized eggs would make females and unfertilized eggs would make males. So the males would miss out on passing on genes to half the female’s offspring.

From Gardner and Ross. Family unit. Our model is based on standard haplodiploid inheritance, with only the female (F) contributing a genome to her haploid son (α son) and with the female and male (M) each contributing a genome to their diploid daughter (β daughter). In addition, the male contributes a genome to infectious tissue that grows in his daughters (δ sons), and the mother’s infectious tissue (T) can fertilize her eggs to produce daughters (γ daughters) and also further infectious tissues (ε sons).

Second, the male will now be able to pass on more of his genes with those mates. Because the eggs he’s fertilizing are from his daughter, who already shares half his genes, he will be more closely related to his granddaughter than if his daughter had mated with some other male. That’s inbreeding in a nutshell. Which genes are coming from which parent is summed up in Figure 1 of the paper (shown at the right).

This sets up a potential conflict between males and females. Females are being forced to make babies with their dads through this parasitic tissue that has obvious benefits for Dad. This is a problem if it would actually be best for the female to mate with other males instead.

But does the female get anything out of the relationship? According to the authors, she must be getting something out of it, or you would expect the “parasitic” male tissue to disappear. Remember, she is related to the sperm-producing tissue (it is her father, basically). So, if it was really bad for her then, because she shares so many genes with the male tissue, it would be bad for the male, too. This would lead to selection for any genes that could suppress the infection of the male tissue.

On the other hand, you might expect there to be some cooperation between the female and the male tissue. Again, these two genomes are closely related, so if the female mates with her “father”, she passes on more of her own genes than if she just mated with a random male. As long as the benefits of passing on more of her genes outweighs the costs of inbreeding for the females, you would expect her to be pretty much ok with the infection.

Males are produced by rare un-fertilized eggs. Females are also extremely rare (if they even exist at all–I was unclear on this point from the paper) and would be produced by an inefficient infection. Basically, the male tissue was able to fertilize an egg, but it wasn’t able to establish a new infection in that egg. The result is a female free of the infection. Because males are so rare, this female is forced to produce haploid males in the hopes (evolutionarily speaking) that they find mates and pass on their mom’s genes for her.

A big question now is: can the rare males in the population also infect females with their own sperm-producing tissue? No one knows this yet, and I hope someone does the experiment!

Another big question also remains: if a hermaphrodite mates with a male, how well does his sperm compete against the parasitic male’s? Basically, do those rare males have any chance at all in producing offspring? I wanna see some sperm competition!

At this point you are probably wondering: how did this infection thing get started in the first place? How do sperm turn into testes inside a female? The authors point to another weird biological phenomenon in this species that may provide an explanation.

The females are infected with a bacteria that gets passed onto her offspring through the eggs. This kind of bacteria is known as an endosymbiont, and these are fairly common (though not universal) in insects. This endosymbiont was shown, in earlier studies, to associate closely with the male sperm-producing tissue.

So, could the bacteria be responsible for protecting the infectious tissue? It would make sense, as the authors point out, because the bacteria benefit if the host only produces daughters. Sons are a dead-end for the bacteria.

Gardner, A., & Ross, L. (2011). The Evolution of Hermaphroditism by an Infectious Male-Derived Cell Lineage: An Inclusive-Fitness Analysis The American Naturalist, 178 (2), 191-201 DOI: 10.1086/660823

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One thought on “Will male cottony cushion scales survive their own mating strategy?

  1. Pingback: Evolution, sex, and spiky penises | Molecular Love (and other facts of life)

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