First of all, apologies for a delayed “Part 3”— my sister is visiting New Zealand and the time for pondering natural history has been channeled into hikes and explorations around this beautiful country. Anyways, the delay in posting means that a recap on Parts 1 and 2 is sorely needed before we jump into Part 3 (the compelling conclusion!). Let’s get to it.
We started this adventure wondering why sexual reproduction would ever evolve, based on the numerical advantage of asexual reproduction. Based on numbers alone, asexual reproduction should be the winning approach. But it isn’t, not always. Sexual reproduction has arisen and flourished across the tree of life. Evolutionary biologists proposed that the advantage of being sexual might come from the variation granted to sexually-produced offspring. That variation provides insurance against a changing future. But where to test that hypothesis? New Zealand, of course! Curt Lively (and the Snail Team) discovered and studied an interesting population of mixed sexual and asexual mud snails in Lake Alexandrina. Over years of monitoring, they’ve found that sexual reproduction consistently remains in the population, while various asexual clone lines follow boom and bust cycles. The most common clone lines grow in population, and then suddenly disappear. The question is, why? It’s likely in response to some external factor, but what external factor could target just the most frequent clones?
Phew! Okay, I think we’re up to date.
We’ve spent some time with the snails and the biologists, but there’s a whole other organism in Lake Alexandrina that is worthy of our attention. It’s even smaller than the minute mud snails, but has a powerful impact on the snail’s dynamics, and is not be ignored.
This mysterious, previously overlooked organism is the trematode of the genus Microphallus. Trematodes are parasites, tiny worms that live in a series of hosts in the lake ecosystem. The key host, in this case, is, you guessed it, Potamopyrgus.
According to the biological definition, a parasite is an organism that lives on another organism at some point in its lifecycle, at the expense of the host. Microphallus has what’s called a complex lifecycle, meaning it relies on a succession of hosts to reach sexual maturity and produce offspring. Briefly: Microphallus exists as an egg in lake sediments, and is gobbled up by an unwitting Potamopyrgus. At that point, the parasite hatches out and starts to produce larvae in the snail’s tissues. Hopefully (from the parasite’s point of view, that is), the snail will be eaten by a duck, delivering these larvae straight into the duck’s intestine, where they’ll meet other Microphallus,and get on to (sexual) reproduction. Reproduction in the duck gut results in eggs that are conveniently deposited in duck poo around the lake sediment. A roving snail, chomping down on the sediment/duck poo mélange, will consume these Microphallus eggs and the cycle will begin again.
By its classification as “parasite”, Microphallus takes resources from its hosts, and necessarily causes harm to the hosts in that process. This happens to varying degrees, however. For the ducks, the harm caused by a gut infection of tiny trematodes isn’t anything particularly drastic. They skim some calories off the duck’s intake, and force some of its energy into an immune response, but ultimately the duck is not obviously hindered.
It’s not the same case for Potamopyrgus. Poor things. Rather than staying in the gut and siphoning nutrients here and there, the trematode in a snail migrates from gut to reproductive structures, starts to divide, and creates a bumper crop of trematode cysts. In this process, it replaces the snail’s digestive tissues and reproductive tissues almost entirely with parasite cysts. This is bad news for the snail, because while it can continue to survive with a gut infection, the gonad infection means it can bid adieu to any hopes of reproduction. A parasitized snail is a sterile snail (and the name “micro-phallus” begins to make some sense…).
That’s the case regardless of whether the snail is an asexual triploid or a sexual diploid. If you get infected, that’s the end of your contribution to the next generation. Ouch.
The host, though, is not a passive player in this relationship. Hosts equipped with genes to avoid or vanquish parasitic infection will do better than their neighbors without those genes. That success can be judged by reproductive output. As parasite-stricken parents flail under the burden of infection, parasite-resistant parents pump out offspring that carry on resistant traits. Gradually, the proportion of resistant hosts creeps higher and higher in the host population.
Sounds like bad news for the parasite, right? But it’s only just getting started. Variation in the parasite population means that some of the parasite offspring just might be able to infect resistant hosts after all. And those offspring will succeed compared to their unable-to-infect-resistants competitors.
So there it is: parasites are under constant selection to infect the most hosts. Hosts are under constant selection to resist the most parasites. Here’s where frequency begins to play into this question. For a parasite to maximize its reproduction, it would do well to infect the most common type of host available. For a host to avoid infection, then, it pays to be rare or unusual, something the parasite has not evolved to infect. Play, and counter play.
It sounds like a game of chess, doesn’t it? Two players, opposing strategies, each strategy continually blocked and readjusted. Except it’s not quite like a game of chess. Chess has an overarching narrative structure to it. It has a beginning, some middle business, and, crucially, an end.
This host-parasite evolution, on the other hand, goes on and on, cycle after cycle. An ending? It doesn’t exist. At any point the two players are essentially right back where they began: a host just barely beating out the parasite, a parasite just barely beating out the host. It’s chess disoriented, stripped of its narrative progression.
And that is why this pattern has been dubbed “The Red Queen Hypothesis”. You know the Red Queen— she’s the domineering matriarch in Alice’s Adventures in Wonderland and Through the Looking Glass, the ruler of the chessboard and the arbiter of arbitrary rules of the land. In her most influential scene, she grabs Alice by the hand and the two start to run, faster and faster, only to find themselves exactly where they started. The queen’s explains, in words that were written first by Lewis Carroll and have since been applied to theories across many disciplines from biology to religion to physics:
Here, you see, it takes all the running you can do, to keep in the same place.
The Red Queen Hypothesis has been proposed not only as an interesting pattern between hosts and parasites, but the very answer to the question we’ve been asking this whole time. Why sex? The Red Queen might reveal it all.
Imagine a new clonal host line. Initially, it’s rare, which means it’s protected from parasites that have evolved through infecting the most common clones. However, the common clones, under the sterilizing pressure of parasite infection, lose their ability to reproduce. The rare clone, then, has a massive advantage. It pumps out offspring unhindered, and becomes more and more successful as the infected clones are parasitized to extinction. Eventually, of course, the rare clone becomes common— and at this point, perhaps, the sexually-reproducing parasite has hit on a genetic jackpot, a combination that can crack the common clones defenses. The next step, of course— all of the common clones are now vulnerable, many are infected, and the clone lineage disappears.
Sexual reproduction mitigates the risk of going bust. In every sexual reproduction event, the offspring have a new genetic makeup. That makes it harder for parasites to co-evolve to such a level of specific, targeted destruction as they do with the asexuals.
Sexual reproduction in the host, then, is a defense against parasite infection. (Or to see it from the parasite’s point of view: sexual reproduction is a defense against host resistance. You can argue it either way.)
And this is exactly what numerous experiments carried out over the years at Lake Alexandrina have shown. Over decades of research, Curt and the Snail Team have gathered remarkable support for the theory that snail lines and parasite lines are constantly evolving in response to each other, each party mutating until they hit on a genetic combination that allows them either to escape parasitism (in the case of the snail) or evade host defenses (in the case of the trematode). The Red Queen hypothesis for the success of sexual reproduction has held steady throughout their findings. Asexual snails are successful to a point, but then the lack of genetic variation makes them vulnerable to complete infection by parasites. Sexual snails create fresh variation in each generation, and have more opportunities to evade parasite infection.
In the Red Queen’s race of co-evolution between parasites and hosts, there’s an advantage to being sexual— you may never outrun your competition completely, but you’ll have better odds of evading it with each lap. In evolutionary terms, that’s enough of an advantage to be a winning strategy.
And so, at long last, we’ve settled on solid evidence for the success of sexual reproduction. And, even better, it’s evidence that ties together chess and children’s literature and NZ fauna into one satisfying metaphor. What could be better than that?
Until next time,
PS: There’s always something to add! If you’re interested, you should definitely check out Curt Lively’s description of the Red Queen hypothesis. It turns out an entire chapter of Through the Looking Glass can be layered with co-evolutionary meaning. Plus, have a fossick (new word! Or is it an old word?) around his website to learn about the more recent snail/trematode findings.