Parasitic Castrators: Introduction

A few weeks ago, I wrote a post that explained the differences between predators, parasites, and parasitoids.  I included a classification scheme that further divides parasites up into smaller groups, including a group called “parasitic castrators.”  For the next few weeks, I’m going to do a miniseries focused on parasitic castrators, because they’re awesome.  Most of today’s post is based on a review by Lafferty and Kuris (2009).

What is parasitic castration?

Rather than reinventing the wheel, I’m going to give you some published definitions for parasitic castration:

Lafferty and Kuris (2009): “an infectious strategy that requires the eventual intensity-independent elimination of host reproduction as the primary means of acquiring energy.”

Baudoin (1975): ‘‘a destruction or alteration of gonad tissue, reproductive behavior, hormonal balance, or other modification that results in reduction in host reproduction above and beyond that which results from nonselective use of host energy reserves by the parasite.”

So, any parasite might reduce host reproduction.  For instance, the host may be temporally too sick to reproduce.  But parasitic castrators specifically target – usually completely eliminate – host reproduction.  Parasitic castrators don’t necessarily immediately sterilize hosts, however.  It might take some time for the infection to mature to the point of complete castration.  And hosts aren’t always permanently castrated – they may regain the ability to reproduce after the infection runs its course, if it ever does.

Stealing Host Energy:   

I like to think about this in terms of pie, because, well, pie is awesome.  Imagine that hosts have some amount of energy that they have acquired by eating stuff.  Hosts have to divide that energy pie among all of their various requirements – maintenance of their current condition, growth, development, reproduction, etc.  For simplicity, let’s just divide the energy pie into energy spent on reproduction and energy spent on “other stuff.”

When hosts are infected by a non-castrating parasite, that parasite ‘steals’ some of the host’s energy pie.  Non-castrating parasites don’t directly affect how the host divides up the pie; they just affect how much total energy is in the pie.  So, we can imagine the pie being divided up the same way, but shrinking.  (Next week, I’ll talk about a really cool modeling paper that explains how non-castrating parasites can indirectly alter the way the pie is divided up.)  Obviously, when the total pie shrinks, the “reproduction” piece of the pie shrinks, too.  The non-castrating parasite may thus reduce host reproductive output without actually targeting the energy that the host spends on reproduction.

Parasitic castrators directly affect how hosts allocate their resources.  Specifically, they stop hosts from spending any energy on reproduction.  One way to think about this is to imagine that all hosts (uninfected or infected) start with the same energy pie, but then parasitic castrators eat all of the energy that hosts would normally spend on reproduction (bottom left pie).  In that case, infected hosts still end up with a smaller overall pie (like what happened with non-constrating parasites), but this time the whole pie is devoted to “other stuff.”

Mechanistically, I don’t think it makes sense to say that castrating parasites only eat as much energy as the hosts would normally devote to reproduction.  (I can’t tell if Lafferty and Kuris would agree with me or not.)  Instead, we’ll say that castrating parasites change the way that the energy pie is divided up, so that none of the energy is spent on reproduction, and then castrating parasites eat some proportion of that pie.   And that proportion may or may not be equal to the proportion that the host would spend on reproduction, if it had the option.

One more point:  for non-castrating parasites, the host’s energy pie always gets smaller.  But for castrating parasites, the energy pie might actually get bigger!  If hosts are no longer spending energy on reproduction, they’re no longer spending any time with behaviors associated with reproduction – finding mates, for instance.  They might just spend that ‘free time’ resting.  But they might also spend that time foraging, which would lead to increased food intake and thus increased total energy in comparison to the energy pie of an uninfected host.  There aren’t any generalizations about when the energy pie should shrink or grow (that I know of), but it probably depends on the host-parasite system and how long the host has been infected.  That would be a cool modeling paper!

Who are the parasites?  Who are the hosts?

Now that I’ve explained what parasitic castrators are, theoretically, I’ll give you some examples.  Trematodes that castrate their mollusk hosts are probably the most well known example, and they are, of course, my personal favorite.  In this case, mollusks are the first intermediate hosts of the trematode parasites.  There’s a cool paper by Hechinger et al. (2009) that found that 13-39% of the “snail tissue” in first intermediate hosts for trematodes was actually trematode tissue!  That’s a lot of parasite!

You might be wondering if humans have any castrating parasites.  The answer is (please, Evolution, don’t try to prove me wrong): nope.  Lafferty and Kuris (2009) argue that our tiny ovaries and testes are probably just too small to be worth eating.  Good hosts for castrators usually need to have a relatively large amount of reproductive tissue and they need to live long enough for it to be worth the parasites’ trouble to manipulate them.  If the host doesn’t have enough reproductive tissue or doesn’t live long enough, it’s probably more beneficial to just eat the whole host, like a parasitoid does.

Here are just a few more examples:

I have previously blogged about Sacculina barnancles and their crab hosts.

Strepsiptera castrate their insect hosts.

The Extended Host Phenotype:

If you’ve followed any of the work about “zombie” hosts, you might have heard of the extended host phenotype.  Lafferty and Kuris (2009) argue that when a host is infected by parasites that manipulate host behavior, it might still look like a host, but it’s actually just a parasite vehicle.  (Just like any organism may just be a fancy vehicle for DNA?)  In fact, they call parasites that manipulate hosts body snatchers, because that’s what the parasites do – they snatch host bodies.

So, the extended host phenotype is the phenotype of the infected host.  And depending on what parasite the host is infected with, the phenotype may change a lot or a little with infection.  With castrating parasites, one common phenotypic change is host gigantism: hosts get much bigger than they would if they were uninfected.  Note that host gigantism doesn’t happen in all systems with parasitic castrators, but it does happen in some systems.

Another phenotypic change that is sometimes associated with parasitic castrators is earlier reproduction by infected hosts.  This is called fecundity compensation.  The common explanation is that if hosts can tell that they’ve just been infected by a castrating parasite, they should quickly produce as many babies as they can before they become castrated.  (I’ll talk more about fecundity compensation next week.)

Finally, you might be wondering how the parasite manipulates the host.  Parasites can manipulate the allocation of host resources by manipulating host hormones.  And Lafferty and Kuris (2009) point out that parasitic castrators might be forced to specialize on hosts in order to evolve just the right tools for host manipulation.

How do parasitic castrators affect host populations?

So far, we’ve only talked about how parasitic castrators affect individual hosts.  But if individual hosts are being castrated, we might expect host population densities to decline because there are fewer hosts reproducing.  And we also expect that the higher the prevalence of infection (and thus the more castrated hosts), the more the host population density should decline.  This is a research topic ripe for plundering!  Now, I don’t want to put words in your mouth, but you might be thinking, “Wow, this population-level stuff would make a fascinating blog post!”  If you’re thinking that, come back in two weeks!

References:

Hechinger, R., K.D. Lafferty, F.T. Mancini III, R.R. Warner, and A.M. Kuris. 2009. How large is the hand in the puppet? Ecological and evolutionary factors affecting body mass of 15 trematode parasitic castrators in their snail host. Evolutionary Ecology, 23(5): 651-667.

Lafferty, K.D., and A.M. Kuris. 2009. Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25(12): 564-572.