Sexual Selection, "Social Selection," and some not-so-hot science

The latest issue of Seed Magazine - the print product brought to you by the same folks who bring you us - has an article about Dr. Joan Roughgarden's work. The main topic of the article is Roughgarden's opinions on sexual selection - she thinks that it is entirely wrong, and that she has come up with a better alternative in the form of something she calls "social selection." PZ Myers took a solid whack at the article earlier this week, and I usually wouldn't waste my time trying to improve on his article - especially when I agree with him. This time, though, I wasn't thrilled with his tone. He was much too kind.

The recent Roughgarden et al. article in Science (Vol 311 Pp. 965-969) stands as a lasting tribute to the not-entirely-infailable nature of the peer review process. Reading it, I was honestly surprised by some of the things that made it into the article. Here's one prime example:

Further, we hypothesize that a sense of friendship resides in animal bonding, a joy or synergy in the spirit of cooperation that allows animals to sense and experience the product, not merely the sum, of their individual well-beings.

One wonders precisely what empirically examinable characteristics this "sense of friendship" might have that would permit this "hypothesis" to be tested. One also wonders if the "sense of friendship" and "joy or synergy in the spirit of cooperation" is present in all animal species that engage in sexual reproduction, or if it is only found in a limited subset of species. Then, of course, there is the question of those animals that are not obligately sexual. Does a starfish experience a "sense of friendship" when it reproduces as a result of fissioning (and if so, with what? The fisherman's knife?) or is the sense of friendship limited to sexual reproduction. Do broadcast spawners get to have the same feelings?

If you look at the list of examples I just provided, you might be able to guess what one of my biggest objections is to Roughgarden's nonsense - it suffers from an enormous vertebrate prejudice. Vertebrates do not make up the entire animal kingdom; we make up a portion of the animal kingdom. We may have a virtual monopoly on the cute and fuzzy niche, but we do not represent either a majority of the species or a majority of the planet's animal biomass. Yet, strangely, Roughgarden seems to ignore the majority of the animal kingdom. From the Seed article:

Roughgarden describes sexual partners as a model of solidarity. "This whole view of the sexes as being at war is just so flawed from the start. First of all, there are all these empirical exceptions, like homosexuality. And then there's the logical inconsistency of it all. Why would a male ever jettison control of his evolutionary destiny? Why would he entrust females to serendipitously raise their shared young? The fact is, males and females are committed to cooperate."

Actually, now that I've taken another look at this quote, I realize that it was a bad example to pick as an indicator of an anti-invertebrate bias - the statement doesn't even have the dubious virtue of being true for all vertebrates. Green Sea Turtles (known as "Honu" here in Hawaii) are one of many examples of vertebrates where neither the male nor the female raises the young. Nevertheless, there appears to be sexual dimorphism in this species, and there is at least some published evidence of sexual selection here1. There is also evidence for sexual selection in species where the two parties are even less involved with each other and their offspring than is the case with the honu - sexual selection appears to play a role in the evolution of reproductive traits (such as sperm and egg size) in at least some species of marine broadcast spawners2,3. Broadcast spawners are organisms that release their sperm and/or eggs into the water column. Fertilization is entirely external, and the individuals involved never know (barring the potential "sense of friendship") if they have managed to reproduce.

Actually, it doesn't look to me like Roughgarden is really talking about sexual selection at all. Just as a refresher, sexual selection was initially proposed, as PZ pointed out, by Darwin as an explanation for why the males and females of a species might differ in appearance, and why certain gender-speciefic traits, such as the Peacock's tail, are so exaggerated. (The formation of such highly exaggerated traits is sometimes referred to as "runaway sexual selection.") The evolution of secondary sexual characteristics has always been a major component of any discussion of sexual selection. Roughgarden, on the other hand, seems to focus on the evolution of mating systems and on cases where sexual activity is used for non-reproductive purposes. Both of these are interesting areas, but they are at best a subset of the areas covered by sexual selection. Roughgarden's treatment of secondary sexual characteristics in the Science paper is somewhat dismissive:

Secondary sex characters are social-inclusionary (SI) traits that permit participating in the species' social system, and exclusion is reproductively lethal. Two types of SI traits include (i) cooperation facilitators like mutual grooming and preening, interlocking vocalizations, between-sex and same-sex sexuality, and other intimacies promoting coordinated team play and the perception of team fitness and (ii) expensive, functionally useless badges like the peacock's tail that are admission tickets to monopolistic resource-controlling coalitions. Any imperfection in an admission ticket is the target of prejudice. In social selection theory, cooperation and team play coexist with prejudice and exclusion.

I'll be somewhat charitable here, and simply say that Roughgarden's attempt at shoehorning the evolution of secondary sexual characteristics into "social selection" is less than compelling. It neglects any number of issues, beginning with the minor point that the connection between secondary sexual characteristics and the material that forms the bulk of the paper is supported by absolutely nothing more than bald assertion and handwaving. It completely ignores the entire question of how such characteristics evolve in the first place. It fails to account for cases, such as sperm and egg competition in broadcast spawners, where describing the traits under selection as "admissions tickets to monopolistic resource-controlling coalitions" is a bit of a stretch. It does not take into account cases, such as in species of Drosophila, where female choice experiments can be, have been, and are being conducted. Hell, it doesn't even do a great job at explaining the Peacock's tail, particularly when compared with the traditional "female choice" explanation.

Now, all that having been said, it is possible that Roughgarden's social selection and the game-theoretic modeling approach employed by her group might be able to explain the evolution of some traits that are not currently well explained by either natural or sexual selection. It seems pretty clear, however, that social selection cannot explain everything that sexual selection can. Any claim - particularly at this early state of research into the hypothesis - that "social selection" has toppled sexual selection is really nothing more than an unjustified explosion of ego.

References
:
1: Godley, BJ et al. 2002. Reproductive seasonality and sexual dimorphism in green turtles. Marine Eco. Prog. Ser. V.226 Pp. 125-131

2: Levitan, DR. 2004. Density-dependent sexual selection in external fertilizers: variances in male and female fertilization success along the continuum from sperm limitation to sexual conflict in the sea urchin Strongylocentrotus franciscanus. Am Nat. Vol 164 pp. 298-309.

3: Marshall DJ, Evans JP. 2005. Does egg competition occur in marine broadcast-spawners? J Evol Biol. V. 18 Pp. 1244-52

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