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Doing it to death: suicidal sex in ‘marsupial mice’

Imagine if you only had one shot at passing on your genes before you died. It happens more often in the natural world than you might expect: suicidal reproduction - where one or both sexes of a species…

After mating, all male Antechinus die … but why? badoo_tealeaf

Imagine if you only had one shot at passing on your genes before you died. It happens more often in the natural world than you might expect: suicidal reproduction - where one or both sexes of a species die after a single episode of mating - occurs in plants and some invertebrates including insects and spiders.

So what about mammals?

In a paper published in the Proceedings of the National Academy of Sciences today, we show why escalating stress hormones during the breeding season of some species of small insect-eating marsupials (but in no other mammals) cause immune system collapse, haemorrhaging, infections and death after mating in all males.

(In contrast to these “semelparous” species, most insectivorous marsupials in Australia, Papua New Guinea and South America are iteroparous, which means that they breed more than once during their lives.)

Parantechinus apicalis. Wikimedia Commons

The lifespan of males after breeding varies between species. About a fifth of insectivorous marsupial species with known reproductive traits have this most extreme condition of complete male die-off through a mechanism of synchronised immune collapse, and comprise four Australian genera:

A different biological clock

These animals typically do not look very impressive and have sometimes been called “marsupial mice”; however, their behaviour and demography is impressive, and nothing at all like that of mice.

As well as dramatic death, these marsupials show extreme sexual behaviour and physiology. In the 12 species of Antechinus, pairs mate for up to 14 hours at a time and both sexes are very promiscuous.

Just before the mating season at 11 months old, something very peculiar and counter-intuitive happens to the reproductive physiology of these males.

Although they have never mated, they stop producing sperm and their testes disintegrate, so the animals must rely on sperm stored in their epididymis (a narrow, coiled tube).

Phascogale calura. Wikimedia Commons

The clock starts ticking for males, because the sperm they manufactured before their testes shut down starts to be lost in their urine. The frenzied mating season lasts only a couple of weeks, and males usually die before young are born.

The manner of synchronised suicide in males is quite horrible to see. Males lose their fur and can develop ulcerations and gangrene.

Biologists used to assume that these animals fight during the mating season but we now know they don’t. Despite the time pressure and rampant testosterone, overt contests between males are virtually absent, and they appear positively friendly towards one another.

In many Antechinus species, males huddle together in nests woven out of gum leaves in tree hollows - groups of both sexes share nests for most of the year.

By the end of the mating season males are active throughout the day, and physically disintegrating males may run around frantically searching for last mating opportunities, but by that time females are not surprisingly avoiding them.

Sperm competition

This situation, unsurprisingly, raises a lot of questions:

  • why don’t males fight?
  • why do they have this bizarre strategy of programmed suicidal reproduction?
  • why do they shut down sperm production before the mating season?
  • why do they show such extreme sexual behaviour?
  • why has this die-off strategy evolved multiple times in insectivorous marsupials but never in any other mammals?

We suspected that the answers to these questions are linked, because all of this is something to do with intense sperm competition.

Sperm competition is a form of post-mating sexual selection in which males compete with their sperm inside the female reproductive tract, rather than fighting to gain access to females.

Sperm competition in mammals is associated with having large testes with lots of sperm-producing tissue, and often also long mating times and mate-guarding.

Competition between males is expected to intensify as the time they have to mate declines, and females synchronise their period of sexual receptivity in time and space.

Australian researchers Tony Lee and Richard Braithwaite, authors of a seminal study published in The American Naturalist in the late 1970s, realised this when they proposed that the seasonality of food is the key factor in the evolution of suicidal reproduction in mammals.

Antechinus babies in a pouch. naked.ape

They thought that these marsupials live in temperate (southern, high latitude) forests, where insects have a predictable peak of abundance at the same time every year, and meaning that females synchronise mating so that young are raised and weaned when this peak of food occurs.

Because even small marsupials have long periods of lactation (months, unlike ecologically analogous placental mammals), they can’t fit in a second litter. Braithwaite and Lee thought that males may as well compete to death to maximise the number of young that they father in the one brief mating season of the year.

Predicting peaks

To test these ideas about the intensity of male contests, the length of the mating season and the sperm competition mechanism, we analysed the habitats, food predictability, demography and reproductive traits of 52 species in 21 genera of insectivorous marsupials, including the four Australian semelparous genera.

We found that insect abundance in Australia, Papua New Guinea and South America shows more predictably synchronised seasonal peaks at higher latitudes than in the tropics at sites where insectivorous marsupials live, and this pattern is not just in forests but everywhere that these animals live.

We also found that seasonal predictability of insect abundance is associated with short, synchronised single mating seasons.

Distribution map of Parantechinus apicalis. Wikimedia Commons

These results indicate that male competition is intensified by short mating seasons, which are driven by seasonal food availability and by the synchronisation of mating by females.

Simply put, competition shortens the life of males. Species with lower male survival (and in the most extreme cases, die-off accompanied by immune system collapse) have larger testes and long mating times, indicating sperm competition.

Mating to death

Small marsupials with suicidal reproduction in males “mate themselves to death” for an adaptive reason. It seems that shutting down sperm production before mating and foregoing any possible future reproduction in order to use all possible energy for mating gives these males an advantage in sperm competition.

Nature documentaries tend to attribute male death before offspring are born to altruistic paternal suicide to avoid food depletion. There are several reasons why this is wrong:

  • Natural selection acts at the level of individuals passing on their genes, not populations of males acting for the good of the species. The genes of males that die and forgo further reproduction for the benefit of young fathered by other males will be disadvantaged.
  • There is no mechanism in these species for males to advantage their own young (“kin selection”), because males range widely during the mating season and litters have several fathers.
  • Mothers do lose weight, but this is nothing to do with how much food they can find; rather, it’s likely to be due to constraints on the rate of converting food to milk. Mothers with unlimited food in captivity also lose weight.

Rather than altruism, individual sexual selection leads to apparent self-sacrifice in these mammals.

Our study suggests that males gain a reproductive advantage from death in a manner parallel to suicidal mating in some spiders such as redbacks, in which males that sacrifice themselves sire more of the female’s young.

Join the conversation

15 Comments sorted by

  1. Peter Ormonde
    Peter Ormonde is a Friend of The Conversation.

    Farmer

    I'm confused ... not uncommon - but having shared my humble accommodations with both antechinus and phascogales I can most certainly assure you that they don't only get one shot at passing on their genes... one short season of non-stop disco parties it is ... a species permanently stuck in the 1980s.... and a very noisy and violent business it is... a pornstar on roids would have no chance of keeping up. Like having the Rolling Stones take up residence in the rafters.

    Live fast, die young and leave a very smelly corpse indeed ... little marsupial party animals... an inspiration to us all.

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  2. Diana Fisher

    Future Fellow in mammal ecology and conservation at University of Queensland

    Yes they have a short intense few days of competitive mating. Lucky you having phascogales at your place, although not if they die in the roof.
    Diana.

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  3. Anika Dell

    Criminologist

    Thank you for the enlightening article, I have been wondering why this occurs. I currently have Dusky Antechinus sharing my home, in fact nesting in the back of the fridge. They collect paper of all kinds for their nest, including Monopoly money, Yu Gi Oh cards and even the empty Ratsak packet. We regularly catch and release, having caught 15 this year so far. At first we were happy to have a few of them to keep spiders etc out of the house, but things turned ugly when they moved from insects to human food. They devoured cereal, brown sugar, taco seasoning, chilli chocolate, crackers - almost anything not in tins or hard plastic. There was also the unfortunate incident where one of them ran up the inside of my trouser leg and bit me on the inner thigh! I can attest to their very sharp teeth and extremely noisy lifestyle, especially during breeding season.

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    1. Diana Fisher

      Future Fellow in mammal ecology and conservation at University of Queensland

      In reply to Anika Dell

      Thanks Anika.
      Yes, they are cute, but not so much if they realise what your food is. Also they make latrines (leave their sticky droppings in one place all the time). Dusky antechinuses are quite big (big teeth) for an antechinus, too.

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    2. Peter Ormonde
      Peter Ormonde is a Friend of The Conversation.

      Farmer

      In reply to Anika Dell

      Yep ... I reckon these critters are well worthy of the attention of criminologists Ms Dell ... watch your sock draw. The time to worry is when things go quiet. Start sniffing about.

      I had a neighbour out in the bush who was boasting how successful he'd been using traps and rat poison to control his plague of rodents. So proud, he'd put the 'trophies' out on a stump to have the ants strip them down to skeletons...about 40 in all ... and each and every one was an antechinus.... tiny little dog teeth, tufty tails ... just mice but innit?

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  4. Geokranium Tropicalis

    Technician and amateur botanist

    Call me juvenile if you must but you just couldn't resist the "seminal article in the American Naturalist" comment could you. :) Deeply interesting article. Unfortunately, great zoological journalism like the example above seems all too rare in the mainstream media. I love it when I find gems like this. Thanks.

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  5. Chris Owens

    Professional

    Nice work! How do you think these conclusions relate to the quolls and even devils which have a very short lifespan compared with other, similarly sized carnivores?

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    1. Diana Fisher

      Future Fellow in mammal ecology and conservation at University of Queensland

      In reply to Chris Owens

      Thanks. We didn't include non-insectivores (they had to eat >50% insects, or the link to insect abundance cycles would be unclear). There is a phylogenetic disposition to fast life histories in dasyurids generally, which is probably related to their high-energy food and relatively small body size. This means they have several young, mature relatively early and don't live as long as more herbivorous marsupials. It may be that the mating competition idea applies to other quolls and devils, and populations with more intense mating seasons have lower male survival. Maybe Menna can comment on that.

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    2. Simon Blomberg

      Senior Lecturer and Statistician at University of Queensland

      In reply to Chris Owens

      The devil facial tumor disease is causing massive mortality, and it looks like very often devils only get to breed once before succumbing to the cancer. This could provide one mechanism to drive the life-table towards semelparity. Whether devils will evolve the complex of traits that lead to male die-off is uncertain. If our model is correct, then females are required to increase sperm competition by decreasing the length of the mating season and timing reproduction to coincide with peak prey availability. Since the diet of devils does not show pronounced predictable peaks in abundance (Menna?), female devils may not be in a position to selectively encourage sperm competition in males. Thanks for the comment!

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  6. Lorraine Muller

    PhD - eternal student

    We had a cinnamon antechinus attacking our quite large cat and I can attest that they are very ferocious. The cat was yowling and trying to get away from the antechinus, so we caught it and put it into fish/reptile tank with a flyscreen lid on it.

    Dubbed David, after the David and Goliath story, we went looking for somebody to tell us what it was - this was before the internet.

    David survived for 12-18 months, fed by our children's insect hunting and cat food, which he ate by very daintily…

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    1. Diana Fisher

      Future Fellow in mammal ecology and conservation at University of Queensland

      In reply to Lorraine Muller

      That's a lovely story. You can prolong their life by isolating males from female pheremones before adolescence apparently, this is what you have done here. The trigger for the cascade of chemical events that results in stress hormones escalating out of control is impeded if they have no contact with females, and other males. Also feeding in captivity delays death a bit, but you would have still been able to tell if he had mated (you would have had to catch him in early October I think for this species).

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    2. Peter Ormonde
      Peter Ormonde is a Friend of The Conversation.

      Farmer

      In reply to Diana Fisher

      Aside from the Jaggerish lifestyle, one of the things that fascinated me about my antechinus housemates was their blase approach to gravity... hurtling about above my bed running along the undersides of rafters and beams, running up window glass and basically getting about the place as if the normal laws of physics simply didn't apply.... like astronauts in zero gravity.

      I could never work out how they did this running upside down business and by the time I got to look at them their feet looked disappointingly normal and dead. How do they do it?

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    3. Lorraine Muller

      PhD - eternal student

      In reply to Peter Ormonde

      I think it could be just pure speed. We know when they are about, by the speed they travel at. They certainly seem to defy gravity.

      Sadly, since Cyclone Yasi we haven't seen any. Perhaps their numbers got knocked around in the storm and subsequent flooding.

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    4. Lorraine Muller

      PhD - eternal student

      In reply to Diana Fisher

      I think it was early October, but the mating season seems to vary slightly depending on the weather I am guessing.

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