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.

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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