“Casanovas are Liars” and the launch of a new open-access science journal
It is well known that higher quality items tend to be more desired, and often more expensive, than their lower quality counterparts. This applies to everything from tomatoes to cell phones to sexual partners. Social species face a quandary if the quantity of preferred items is limited, however, and competition is especially intense if members of that species commonly mimic each other's choices. For example, if you express a preference for something, you are indicating that you think it's relatively valuable. Soon, everyone will want that same highly desirable item (or others just like it), and the increase in competition will hurt your likelihood of monopolizing the resource for yourself. What to do?
One option is to fake it. If you are vigilant about when others are observing and imitating your choices, then you can act as though you prefer X, even when you actually prefer Y. This will make others eager to obtain X as well, leaving you with Y all to your manipulative self.
Anyone who ever had to endure high school knows that humans are tricky and manipulative, but would a non-human animal be capable of pulling off such a deception? A new study by a team of researchers from the University of Frankfurt and the University of Oklahoma suggests that fish may indeed display this strategy of “deceptive mate choice” in order to decrease male-male competition for mates. Their results have been published in a brand new open-access science journal, F1000 Research (Bierbach et al. 2013).
As we learned from my recent post about a study on posthumous fatherhood among Trinidadian guppies (Poecilia reticulata), poeciliid fish experience significant sperm competition. After copulation, females can store sperm to use later, meaning that sperm from multiple males co-exist and compete within the female’s body. There is evidence for a recency effect (more recently injected sperm is more likely to be used to fertilize eggs), so increasing the amount of time between copulations will increase the probability that the first male’s sperm will "win."
Thus, a male poeciliid has a very good reason to lead other males away from his preferred female. If he can prevent—or even delay—her copulation with another male, then he can improve his odds of fathering her offspring. Poeciliids are known to mimic each other’s mate choices, which means that by the very act of copulating with his first-choice mate, a male may have encouraged his rivals to do the same. It’s a poeciliid predicament.
If a male fish were to be tricky, though . . . he could mate with his preferred female, then turn around and mate with a different, less desirable one, to try to divert the attention of rival males away from his first choice. A little bit of deception could go a long way, when it comes to avoiding sperm competition.
Bierbach and colleagues designed a study to test this hypothesis. They conducted experiments to determine whether more sexually active species—which are most likely to have mating systems involving sperm competition—were also more likely to change their mate preference when they have an “audience” of another sexually mature male. The study was fairly straightforward. Bierbach and colleagues obtained data from 10 types (subspecies and ecotypes of some species were counted as different “types) of poeciliid fish. First, the researchers determined whether male sexual activity (determined by quantifying the number of sexual behaviors displayed during mate-choice trials) and male aggression was consistent within species. In other words, do all males of Species X display similar levels of aggression and sexual activity? They then evaluated whether the species differed significantly in these behaviors. Does Species X act more aggressive or sexually enthusiastic than Species Y?
Next, they tested to see whether the two behaviors are correlated across species—in other words, are more sexually active species more aggressive than less sexually active species? Finally, they compared the magnitude of “audience-induced” changes in mate choice across species. Then, the ultimate question: if there are differences in deceptive mate choice between species, are the more deceptive species also the more aggressive and/or sexually active species, as hypothesized?
Before we dive into the results, let’s review why the study was done this way. Deceptive mate-choice behavior (called “audience effects” in this study) may not be entirely explained by sperm competition. It could be that a male is trying to avoid an aggressive encounter with another male by selecting non-preferred females when rivals are around. He may be more of a wimp than a trickster. This is why Bierbach and colleagues also tested whether a species’ level of male aggression was correlated to sexual activity and/or audience effects in mate choice.
The results are best summarized in the title of the journal article: “Casanovas are liars.” The results indicate that male poeciliids are indeed tricksters: focal males showed significant “audience effects” in nine of the ten species that were tested. Interestingly, the consistency of audience effects did not differ significantly between species, meaning that species were equally predictable in their utilization of the deceptive strategy, even though all not all species employed it at the same rates.
There was a positive correlation between level of sexual activity and the likelihood that a male fish would show audience effects in his mate choices, upholding the authors’ hypothesis that males at higher risk of sperm competition from rivals will face more pressure to be deceptive.
There was also a positive correlation between aggression and level of sexual activity. This is likely related to hormones—elevated corticosteroids (testosterone and its derivatives) in the blood of more sexually active males can lead to heightened aggression. Intriguingly, although more sexual activity was positively correlated to audience effects (remember, this means the rate at which the fish varied their mate preference with and without and audience), aggression alone was not a significant predictor of audience effects.
One novel aspect of the new journal this study was published in, F1000 Research, is that it publishes the reviewers’ comments right along with the paper itself. Thus, we are able to see valuable comments and perspectives from the professionals that reviewed the paper. For example, this paper’s reviewers re-emphasize one caveat the authors point out regarding the nature of this study—the analyses show correlation, not causation. Thus, further research is needed to unveil the exact mechanisms driving the behavioral patterns documented in this study.
One reviewer points out a plausible concern: what if a male doesn’t necessarily shift his mate preference in order to deter a rival, but instead shifts his attention to another female because a female’s chance of mating is reduced for a period of time after he copulates with her? In other words, if she enters a refractory period, he can go to his B-list of options without much risk of a rival immediately copulating with his favorite mate and interfering with his sperm’s activity. I also wondered whether Bierbach and colleagues' metric of "sexual activity" actually corresponds to the average number of mates and/or the degree of sperm competition between males. Investigating these (and other) issues will require further studies, but it’s good to keep multiple explanations in mind when assessing the causes of any kind of animal behavior.
This paper is noteworthy for another reason beyond its interesting results: it was included in the first wave of articles published by F1000 Research, which is taking an innovative new approach to the publication of life sciences research. Here are a handful of the journal’s noteworthy features:
1) The journal posts papers immediately—no more waiting close to a year (or more) to see a submitted article in print. This goes for official, data-driven research results, scientific opinions, and comments on previously published work. This creates huge potential for real-time scientific discourse.
2) All authors are required to submit the entire dataset used for each study. This is the epitome of open-access: if you question the findings of a paper, you’re free to re-analyze the data yourself or check for ways that the chosen statistical methods may have influenced results.
3) Peer review is still conducted, albeit after the article is first published. This means that the entire scientific community has access to the initial ideas and methods presented by the researchers as well as other experts’ responses and critiques. If a paper is of low merit, you’ll be able to see why and use it as a learning experience, and can still obtain some valuable ideas from the hypotheses that were posed and the reasons that the results did not pan out significantly or as expected. This process of public criticism will also (hopefully) function as a quality-control mechanism.
I actually planned to publish this post over two weeks ago, but decided to wait to see the second of reviewer comments, as the paper hadn’t been officially “accepted” when it was first posted on F100Research’s website.
4) Peer-review is not anonymous. Every referee has his or her name and affiliation attached to their reviews.
5) All articles are freely available to the public, rather than hidden behind hefty subscription fees and institutional access limits.
F1000Research is also open to publishing non-traditional items, which are often neglected in more traditional journals despite their potential value. This includes a host of article types, including null/negative results, replicate analyses of previous work, and field observations or other reports that are not data-driven, but may be useful for stimulating ideas and discussion within the scientific community.
Is this a viable model for a scientific journal? Are all of these principles improvements on the way we conduct, publish, and read about science? It is certainly an intriguing experiment that will be worth following. As the push for more open-access science literature grows, publications such as PLoS and the Frontiers network (supported by the Nature Publishing Group) have shown that open-access journals can be successful and attract high-quality work. I highly encourage you to head over to the new journal's website and see what you think, and be sure to offer your comments on how you think the open science movement can be improved!
Bierbach, D., A. M. Makowicz, I. Schlupp, H. Geupel, B. Streit, M. Plath. 2013. Casanovas are liars: behavioral syndromes, sperm competition risk, and the evolution of deceptive male mating behavior in live-bearing fishes. F1000 Research, 2:75 DOI: 10.12688/f1000research.2-75.v1