Hacking Sex – The Odd Lives of Sexual Parasites

Female Amazon mollies need to mate with a male to reproduce. On the face of it, that’s not a terribly surprising statement – it’s on par with “Humans breathe air.” But the tricky secret of these strange fish lies in the details.

Amazon mollies, technically known as Poecilia formosa, are a hybrid species composed entirely of females. Sometime around 280,000 years ago, in a river or stream geneticists have pinned rather specifically to the vicinity of Tampico, Mexico, a pairing of a sailfin molly (Poecilia latipinna) and an Atlantic molly (Poecilia mexicana) resulted in a new fish lineage that has since relied on males of both those ancestral species to mate. And here’s where things get weird. The piscine male mates usually don’t contribute any genes to the Amazon molly offspring. Amazon mollies require sperm to kickstart the development of their embryos, which are genetic clones of their mother, but the male’s genetic contribution is totally wiped out. Amazon mollies are sexual parasites.

The phrase “sexual parasite” might conjure up memories of unpleasant exes, or the irritating hitchhikers that rely on intimate liaisons to jump ship between hosts, but the term truly signifies unusual, ephemeral species that exploit other individuals to propagate their own genetic legacy. Beyond that basic principle, though, the details of sexual parasites are a bit squishy. In species with distinct males and females, there can be sexual parasites of either sex. Whereas Amazon mollies block the genetic contribution of males after mating, males of some ant species – such as the longhorn crazy ant – are capable of leaving behind genetic clones of themselves by fertilizing eggs that would otherwise hatch as females. But there are hermaphroditic sexual parasites, too, including some planarian flatworms and Tassili cypress trees. So far, researchers have identified about thirty genera of sexual parasites, belonging to eight phyla. There may very well be more as-yet-undiscovered examples.

Sexual parasites are able to take advantage of other individuals, whether belonging to the same species or a closely-related one, by one of two strategies. In some cases, the reproductive trick is immediate. Either the egg of the parasitic species discards the genetic material in sperm (except in cases of the awkwardly-termed “paternal leakage”), or, in the case of male sexual parasites, the genetic material inside sperm hack a female’s eggs so that only the male’s genes are passed down. For some organisms, though, sexual parasitism takes a slightly more circuitous route called hybridogenesis. In this process, egg and sperm actually fuse, and the resulting offspring has genes from both parents. But through subsequent cellular processes, the genes of the host parent are discarded, leaving only the parasite’s genes to subsequently be passed down. For victims of sexual parasitism, when genetic unfairness kicks in is only a matter of time.

Despite being successful evolutionary tricksters, though, sexual parasites are typically short-lived species that evolve either from hybridization or mutations to processes such as cell division and sperm generation. Rather than having deep histories, Australian National University biologist Jussi Lehtonen and colleagues argue in a new Trends in Ecology and Evolution review, sexual parasites are “scattered across the tips of the tree of life.” That’s because ill-gotten reproductive benefits accrue major costs over time. Lineages of clones rack up harmful mutations, which may make sexual parasites more susceptible to disease and abnormalities in a “mutational meltdown.” And, among species in which individuals are male or female, the success of sexual parasites might deplete the pool of the hosts required to keep the reproductive cycle going. How these costs and benefits are balanced through the economics of sneaky sex isn’t totally clear, although some sexual parasites have become intertwined with their hosts in unusual ways.

The basic outline of the Amazon molly’s behavior would seem to reflect a fish that is conning male mollies out of their reproductive legacy. But the picture isn’t actually that simple. The Amazon molly plays an unusual role in even normal reproduction of the host molly species.

Experiments involving male mollies, females of their species, and Amazon mollies have found a distinct “audience effect” – male mollies seen in the company of Amazon mollies were found to be more attractive to females of their own species. Male mollies may even use Amazon mollies to trick competing males. Given a choice between a receptive Amazon molly and a molly of their own species, male mollies prefer their own kind. But if another male is watching, the choosy male will often pick the Amazon molly first. Could this be an example of the choosy male trying to throw his competitor off the trail, therefore having more time to then mate with a female that will actually pass along his genes? That’s difficult to say. Nevertheless, despite the minor costs of males mating with sexual parasites, being seen around Amazon mollies may actually have reproductive benefits for male fish.

Sexual parasites are organisms betwixt and between the extremes and sexual and asexual reproduction. By combining aspects of both, the organisms play into the ongoing arithmetic of evolution in which cost and benefit is ultimately judged by how long your genetic lineage lasts. And even though sexual parasites might be characterized as “selfish” organisms, their hosts are not simply left to be cheated out of their reproductive legacy. Sexual parasites change the behavior of their hosts, spurring a wandering evolutionary unfolding from one generation to the next. Still, I can’t help but think that it’s fortunate that our species isn’t involved in the confusing and complicated dance of sexual parasitism.

References:

Fischer, C., Schlupp, I. 2010. Feeding rates in the sailfin molly Poecilia latipinna and its coexisting sexual parasite, the gynogenetic Amazon molly Poecilia formosaFeeding rates in the sailfin molly Poecilia latipinna and its coexisting sexual parasite, the gynogenetic Amazon molly Poecilia formosaFeeding rates in the sailfin molly Poecilia latipinna and its coexisting sexual parasite, the gynogenetic Amazon molly Poecilia formosaFeeding rates in the sailfin molly Poecilia latipinna and its coexisting sexual parasite, the gynogenetic Amazon molly Poecilia formosa. Journal of Fish Biology. 77: 285-291

Lehtonen, J., Schmidt, D., Beubel, K., Kokko, H. 2013. Evolutionary and ecological implications of sexual parasitism. Trends in Ecology and Evolution. (In Press)

Schlupp, I. 2010. Mate choice and the Amazon molly: How sexuality and unisexuality can coexist. Journal of Heredity. 101 (Supplement 1): S55-S61