I was going to call this post “Australian mammals screw themselves to death,” but I thought that might be a bit too salacious for a title. But it accurately conveys the content of a new paper in the Proceedings of the National Academy of Sciences by Diana Fisher et al. (reference and download below). (You can see a short popular description of the work at D-Brief on the Discover blog network.)
The observation at issue is that in several species in four genera of small marsupials from Australia and New Guinea, males mate only once, or with several females over a very short period. They copulate frenetically and for long periods (mean 9.4 hours but up to 14 hours per bout!) and then drop dead immediately thereafter, their immune systems shot to hell. (Females live longer.) More than 90% of the males die almost immediately after mating, so that the population loses nearly all its males in synchrony. The reproductive system of mating only once in a lifetime is called “semelparity,” while animals that have several reproductive episodes over their lifetime are said to be “iteroparous.”
The males show a number of features for this one-shot, suicidal reproduction. They irrevocably shut down the production of sperm about a month before the short breeding system, and begin losing sperm through their urine, so they must inseminate a female soon lest they become permanently infertile and die without issue. The breeding season is short (about a month), occurring right around the peak of insect abundance in the marsupials’ habitat.
Here’s one of the marsupials that does this: the “phascogale” from Australia (there are two species in the genus Phascogale, also called “wambengers”):
Why do the males kill themselves over sex? The authors list several previous suggestions for this well-known phenomenon, including unknown “developmental constraints” that make the behavior nonadaptive, as well as “altruism” (“males sacrifice themselves to avoid competing with the next generation for limited food”). The latter explanation seems unlikely, as it depends on group selection—a process not known to account for any adaptations in nature.
The authors suggest that suicidal reproduction is adaptive in an environment where the breeding season is short and predictable. First the seasonal predictability of insect prey should be higher in these mammals’ habitat (high latitude forests and grasslands) than at lower latitudes where the suicidal species don’t live, and those peaks would coincide with the time females produce offspring. Further, females would have shorter breeding seasons in species having suicidal males, and that the breeding season of species with suicidal males would be shorter than those having males that reproduce more iterparously. Such findings would support the idea that female reproduction is constrained by the environment, and that males have only one real chance to mate before females can produce their (and the males’) offspring.
These predictions were all confirmed. Note that while these findings support the theory, they don’t constitute what I see as extremely strong evidence.
Here’s one figure showing that the length of the breeding season is correlated not only with the predictability of insect abundance (greater predictability, shorter breeding season) as well as with the “suicidality” of males. Each number indicates one species of insect-eating marsupial, with “1” being those in which more than 90% of the males die after mating, ranging through “5”, fully iteroparous species, with intermediate numbers indicating intermediate levels of male die-off. As you see, the shorter the breeding season, the greater the synchronous die-off of males, as predicted:
The authors conclusions are below, noting the analogy to suicidal reproduction in male spiders. Males in some spider species appear to “voluntarily” catapult themselves into the female’s mouth after mating, giving her a meal that enables her to produce more baby spiders (that behavior has been shown by experiments to be adaptive in males, since those males making the fatal legspring produce more offspring):
An adaptive hypothesis to explain why insectivorous marsupials are prone to evolve lethal male competition is strongly supported by our comparative data. . . Strong sexual divergence in reproductive lifespan also occurs in some spiders, in which sexual selection has led to adaptive suicidal reproduction in males of at least one species because cannibalized males manipulate female behavior to increase paternity. We propose that in semelparous marsupials, females manipulate male behavior to increase their own reproductive success. Males in seasonally predictable habitats increase mating effort at the expense of survival, not because adult male or female survival is low for environmental reasons in these habitats (which are relatively benign and predictable) or because males are altruistic, but ultimately because females profit from sperm competition. Environmental seasonality sets the scene for females to impose severe sexual selection pressure on males by shortening the breeding period and mating with extreme promiscuity.
Now I’m not sure if there are data from these species showing that females who mate repeatedly have more offspring. If that wasn’t the case, then it’s not kosher to say that females are “manipulating male behavior.” Even if females mated only once, and the mating season were short because of a spike in insect availability, males might still compete frenetically with other males to mate, and might die in the attempt—but it would be controlled more by the environment than by “female manipulation —although access to females is still crucial. And we still don’t know why these males don’t live longer than a year, getting a chance to produce offspring the next season. Perhaps their small size and high metabolism gives them a short life span.
But I suspect that the authors are right here. To make their conclusions firmer, we need to know whether females in the “suicidal” species mate more than once, and whether those who do have more offspring. We also need data showing that males who mate with already-mated females have offspring, rather than just wasting their sperm. That’s certainly true in the Drosophila I work on, in which males who mate with previously-mated females actually “displace” the previous males’ sperm, producing the lion’s share of offspring. That gives an evolutionary impetus to mate frenetically and repeatedly—which they do.
After all this, what can you say about those males but “what a way to go”? Sadly, you can’t even say that the males who mate themselves to death die happy, as happiness is probably a concept foreign to these small marsupials. What you can say is that they’ve done well by their genes.
h/t: Diane G.
__________
Fisher, D. O., C. R. Dickman, M. E. Jones, and S. P. Blomberg. 2013. Sperm competition drives the evolution of suicidal reproduction in mammals
Proceedings of the National Academy of Sciences, early publication, 10.1073/pnas.1310691110
None of the evidence presented actually tests whether death after single-mating is adaptive (superior to death after multiple mating). The critical prediction of this hypothesis is that males exhausting themselves by single mating (i.e., males not retaining resources to live longer and have a chance at a second mating) have higher fitness compared to other males retaining resources in order to live longer and mate multiply.
Multiple mating vs single mating of females is largely irrelevant (depends, for example, on sex ratio in mating pool). The data showing latitudinal gradients and correlations with breeding-season length is not conclusive evidence (it is consistent also with other hypotheses predicting these trends); I agree with Jerry here.
Not having read the paper (apologies to the authors), it sounds as if this is another study that may have been published in a high-profile journal because of the expected coverage it will receive in the popular press, and the hype it will generate in the blogosphere.
Luckily, as we all know, WEIT is not a blog.
“What a way to go”, indeed.
This reminds me of the cartoon show “Futurama” in which the gang finds out that Zoidberg, the alien lobster character, is part of species that dies after they have sex. “Now that’s a tough choice.” Said Fry (another character on the show).
By the by, I’ve written a post on evolution, creationism and biogeography that I think you guys will find interesting (my blog is linked through my name). I managed to dig up the only creationist explanation of biogeography that exists (as far as I know) and it is truly bizarre. The post also makes excellent ammunition against creationism, if you need any.
Cheers!
” Sadly, you can’t even say that the males who mate themselves to death die happy, as happiness is probably a concept foreign to these small marsupials.”
So, is it safe to say that the males may not even care if they are coming or going?
Nice one, Ginger.
If it was the case that in similar species both adults died after producing offspring (or fertilized eggs, like salmon), I’d suggest that these species evolved from a similar line, in which it was the females then evolved to stop suicidal reproduction.
I don’t think this is the case, but I throw it out to practice thinking from other perspectives.
In all small marsupial insectivores, mortality is very high all the time and especially just after reproduction. Your perspective may be the right one.
Just to take a break (well) from the sex jokes, I note that “semelparious” always tickle my swedish part of the brain. Since we appreciate the eating of “semlor” (hot walls) yearly in a short burst of “semmel-ätande (semmel-eating)”, does that mean our bakers are “semleparious/semmelparious”?
_parous_.
Perhaps the poor things have some other advantageous adaption and this one came with the package and persisted because they successfully reproduce regardless.
All the lady marsupials must wonder, “why don’t they ever call?” 🙂
They don’t call because they are “wambengers” as in “wam beng thank you maam”….. god that was a terrible attempt at a pun!
🙂
You made my day.
I’m very dubious about the regression line in that graph. If the line was calculated using least squares, then a few observations at the upper right are having undue influence.
It would interesting to see what the regression line would be if calculated using L₁ regression, where the sum of the absolute values of the residuals is minimized, not the sum of squares. (L₁ regression tends to discount outliers.)
Because of the very short breeding season, a male would have zero chance of breeding a second time until he is fully two years old, which seems to be getting near the max lifespan of these critters. If the mortality during the second year is high enough, it is better to give it all you’ve got the first time around, rather than have a small chance of mating twice. My thinking is that there is no advantage at all for males to increase their lifespan to any point between 13 months and 23 months, because they wouldn’t breed anyway. The females have to live longer of course, to raise the babies.
Exactly. We’re surrounded by thousands of species for whom this is the norm – nearly every species of insect. The unusual thing here is that it occurs in a mammal.
I’d agree that a large majority of insect species are abruptly semelparous, but survival into a second [or more] year of reproduction appears to be fairly common in some groups –perhaps best documented in predatory ground beetles [Carabidae].
So not “nearly every species”
From a selfish gene standpoint, isn’t more adaptive to be efficiently widespread rather than overwhelmingly widespread. In other words, it pays off to have just the right number of copies of a gene in a given environment rather than too many or too few. Females that selected for males that literally screwed themselves to death would discover over time that their offspring are better off without their dads eating food that would be better used by their offspring. These seemingly maladaptive traits like altruism or death by buggering are mechanisms that permit a gene to find its optimal number for survival and reproduction. I suppose it is similar to the way clutch size is determined. It would seem advantageous for an individual to buck the trend and increase clutch size over its neighbors, but in trying to raise more chicks, less survive when times are tough.
If it is almost certain that a male will die before he is two years old no matter what he does, why not be suicidal and invest everything in sperm and mating on the chance of having an additional son or daughter. Once semelparity gets going, selection will favor increasingly extreme investment in sex. A promiscuous ancestral mating system in would help things get started by assuring a correlation between sexual activity and offspring number. Mammals are for the most part promiscuous. Insectivores may have a harder time surviving winter. I would bet that many year-old females starve during winter and that embryos do not become demanding until well into spring.
This suicidal behavior reminds me of the “sexual cannibalism” in the praying mantis.
That picture’s actually of a Planigale, not Phascogale. Planigales are the smallest marsupials (at least in Australia) and adapted for hiding and foraging in narrow crevices, with flat head and splayed hindlimbs. Phascogales are squirrel-sized and arboreal, and much more charismatic.
Dependence on high latitude and highly predictable seasonality of food… doesn’t seem to fit with Quolls (Dasyurus), where the only (partially or ‘facultatively’) semelparous species is the Northern (i.e. low-latitude, tropical) Quoll D. hallucatus. It’s bigger than other species with die-off, but the smallest member of the genus and probably sister group to the several larger southern/eastern species, so it seems quite possible that semelparity is retained in this species from small ancestors (which doesn’t require an adaptive explanation!) but has been secondarily lost in the high-latitude part of the continent.
I’m not sure how ‘Colwell’s P’ is measured, but should check it out because the maximum value ‘1’ is reported for sampling sites both in Brisbane (humid subtropical east coast) and the Pilbara (arid zone, wet/dry monsoonal climate and high frequency of cyclones). The short mating season and male die-off in N. Quoll certainly do not correspond to the main peak of insect abundance, which is typically in January (depending on cyclones etc.), when juveniles have already dispersed but are months away from maturity. The model may work fine as a generalization for the small forest species, but every species is an individual.
sub
You wrote: “The latter explanation seems unlikely, as it depends on group selection—a process not known to account for any adaptations in nature.”
Should I interpret this comment to indicate that you fundamentally disagree with the view presented by E.O. Wilson in “The Social Conquest of Earth”, that Multi-Level Selection – which includes group selection – is largely responsible for the evolution of humans as currently constituted?
Sure looks like it: http://whyevolutionistrue.wordpress.com/2013/02/26/e-o-wilson-mistakenly-touts-group-selection-again-as-a-key-factor-in-human-evolution/
As the English politician John Wilkes said, “Life can then little else supply but a few good fucks and then you die.”
Reblogged this on Mark Solock Blog.