F Rosa Rubicondior: Selfish Genes and Attractive Cannibals

Saturday 15 March 2014

Selfish Genes and Attractive Cannibals

Pennsylvanian grass spider Agelenopsis pennsylvanica
Zoologger: Female spider kills male to attract a mate - life - 11 March 2014 - New Scientist

Examples of females eating their mates during and after mating are well known in the animal world especially amongst the carnivorous insects and arachnids, like the praying mantis and the black widow spider, but it's rare to find an example of where this tendency actually makes the female more attractive to the male. In fact, at first sight, this would appear to run counter to what evolutionary theory tells us should happen.

But, with a little bit of thought and application, it is quite possible to come up with perfectly rational scenarios where this is exactly what evolving 'selfish' genes might produce. It might also be an example of evolution in progress where competing strategies might not have produced a winner yet.

I can't for the life of me see how it can be explained as the intelligent design of an all-wise and all-loving creator though. Maybe there is a creationist who can help me out here by suggesting one other than by invoking the universal cop-out that we can't hope to understand the mind of this magic creator but we should just accept that it's all for the best, because everything done by God er... The Intelligent Designer is perfect.

This particular example involves a harmless (to humans) common spider - Agelenopsis pennsylvanica or Pennsylvanian grass spider - which inhabits the northern United States down to Tennessee and Kansas. The species is one of the largest of thirteen similar Agelenopsids which live in grass and make a sheet web with a funnel at one end leading to a hole in the foliage, where they hide. The web isn't sticky like most spider webs but the spider is fast and rushes out of the funnel to grab any passing prey which walks on the web so alerting the owner to its presence.

But, to get to his potential mate, a male A. pennsylvanica needs to get across this web and close enough to the female to deliver his sperm package without triggering the attack response in his mate. Unfortunately he often fails and ends up as a meal.

Unlike the black widow where at least mating often takes place before she eats her mate, and the mantis where it normally at least gets under way, then the male makes do without his head as the female reaches round and eats it, finishing the rest off later when mating has finished, most male A. pennsylvanica who get eaten get eaten on the initial approach. Field studies have shown that, in urban areas, females are approached between zero and three times by males in the three-week breeding season so eating them seems a shortcut to extinction by celibacy yet 38% of females eat the first male to approach.

Now a team led by Jonathan Pruitt of the University of Pittsburgh in Pennsylvania, USA, has shed some light on what's going on here. They captured 100 wild females and divided them into two groups of 50. One group were fed wounded males; the other crickets - their normal prey. Between 20 and 24 days later they gave 20 male spiders a choice of females. 75% of them picked the females which had eaten a male.

They also found that the cannibal females produced more and better quality eggs which were more likely to hatch. They had obviously got some nutritional benefit from eating a male. The key finding however was that females normally only eat one male after which they can be approached with relative safety. 38% of females ate the first male to approach them but only 5% ate a second male. They seem somehow to be sending out the message that they have already had lunch to prospective mates.

Precopulatory sexual cannibalism is an extreme form of sexual conflict that can entail significant costs to the cannibalized individual and a variety of costs and benefits to the cannibal itself. Characterizing these costs and benefits is fundamental to our understanding of how this behavior evolves. Using the spider Agelenopsis pennsylvanica, we tested the reproductive consequences of precopulatory sexual cannibalism by staging cannibalization events and comparing the performance of experimental cannibals against natural cannibals (i.e., those that cannibalized on their own) and non-cannibals. We found two performance benefits associated with precopulatory sexual cannibalism: first, experimental cannibals were more likely to produce egg cases than non-cannibals, and second, egg cases from experimental cannibals and natural cannibals were significantly more likely to hatch than those produced by non-cannibals. We then tested whether males were more likely to approach the webs of experimental cannibals vs. non-cannibalistic control females. Our data demonstrate that sexual cannibalism increases female attractiveness to males. Although this result seems counterintuitive, in fact, rates of precopulatory sexual cannibalism were much lower in females that had already cannibalized their first male: 38% of sexually naïve females engaged in precopulatory sexual cannibalism, whereas only 5% of females engaged in cannibalism a second time. Thus, males that approach cannibals receive two benefits: they are less likely to be cannibalized precopula, and they have the possibility of mating with females that have a higher probability of producing viable egg cases. Taken together, our data suggest that precopulatory sexual cannibalism affords females numerous benefits and may have a hand in shaping male mate choice decisions.

Pruitt, J. N., Berning, A. W., Cusack, B., Shearer, T. A., McGuirk, M., Coleman, A., Eng, R. Y. Y., Armagost, F., Sweeney, K., Singh, N. (2014),
Precopulatory Sexual Cannibalism Causes Increase Egg Case Production, Hatching Success, and Female Attractiveness to Males.
Ethology. doi: 10.1111/eth.12216

So what's going on here?

Well, the gene theory of evolution tells us that whatever 'strategy' produces more copies of genes in future generations will come to predominate in the species gene pool. It seems that, like black widows and mantises, providing the female with a free meal from which she can build more viable eggs will produce more surviving copies of the male genes. Males play no part in rearing the offspring and have no utility value to either female or offspring. The genes have no concern for the individual welfare of their carriers so these extreme forms of altruism can be expected in the right circumstances.

So, at some point in their evolutionary history, A. pennsylvanica probably went through a stage in which males were eaten postcopula by a percentage of females. Meanwhile, with no way of knowing whether the female was a cannibal or not, males had no choice but to run the risk (not that this is a conscious decision, of course), but if the offspring acquired some advantage there was not only no evolutionary pressure to do away with cannibalism but there may well have been evolutionary pressure to retain it.

Then, with a ready supply of males, there was some advantage to the females in eating the first male before mating - maybe the additional time to assimilate whatever they got from them before producing eggs. These over-eager males were now at a significant disadvantage because they provided sustenance but not to their offspring so there was now a much stronger reason for males to avoid cannibal females in terms of perpetuation of their genes.

So, males had a reason to evolve ways of discriminating and females had a reason to evolve ways of overcoming this tendency and they had the means - they could use something from their dead suitor to signal to the males that they were now safe to approach. So, females who provide this signal and males who can detect it and respond to it, both derive a benefit in terms of more high-quality eggs and more offspring carrying the genes for it.

This system appears to give a significant advantage to females and to males who wait for the safety signal, so the fact that 62% of females are not cannibalistic suggests there are ongoing evolutionary arms races here between different strategies. Males appear to have two strategies - to make an early approach which is successful in 62% of cases but the eggs are of lower quality, or wait for the safety signal and be successful with the remaining 38% of females but with better quality eggs. Meanwhile females also have two different strategies - eat the first male and produce more high-quality eggs with the second if one comes by and if it detects your signal, or mate with the first one and produce lower quality eggs. Self-evidently, the system can't move to one where all the males play the waiting game because that strategy would be bound to fail. If it happened locally, that population would go extinct, so removing all their genes from the gene-pool.

It may well be that the arms races simply haven't run their course yet, or the different competing evolutionary drivers have arrived at an equilibrium, but we may be seeing evolution in progress here. We are certainly seeing evidence of selfish genes doing what selfish genes do - making copies of themselves with no regard to what effect their strategy for doing so has on individuals, just so long as it gives the most copies.

Any creationist prepared to take up my challenge or will it be silence again as usual when faced with real examples of real evolution instead of the usual infantile parodies you normally attack?

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