Back is black

The darker the better ?

A common way to communicate in animals, actively or passively, is to use visual cues. Such cues can provide information on your energetic status, your motivation, your origin. Some pigments are widely used in many animal species, such as melanin. Melanin is a trait characterized by an important heritability, and it has been shown to co-vary with many traits of importance for evolutionary ecologists: stress, dominance, immunity or reproductive investment.

This might be so because of at least two non-mutually exclusive reasons: first, the genes that code for melanin production can be pleiotropic, therefore also controlling for other traits. Second, the genes that code for melanin are associated with genes that code for other adaptive traits, due to a possible genetic correlation shaped by natural - or sexual - selection : if melanin production is a honest signal for adaptive traits, then it may have been picked up by the other sex as a cue for selecting the best mate, therefore creating a correlation in the association of alleles between the melanin genes and other genes coding for adaptive traits.

Because melanin has an apparent strong genetic basis in many species, and because we can determinate melanin level relatively easily without killing individuals, it has become really popular among evolutionary biologists, and several publications have reported correlations between melanin production and traits of interest for fitness [1].

Vincent Roussille worked in our lab during his Master degree, in collaboration with Lisa Jacquin. Together, they investigated the matter of melanin production and correlations with other traits. To do so, they wandered along two different avenues, the first of which we will browse today. They decided to benefit from an already completed experiment in sexual selection led by Marine Freychet in 2010, a former student in our lab. Simply put, Marine had placed brown trout spawners in a semi-artificial experimental channel, and observed reproductive behaviour (more to come on this soon !). Vincent and Lisa used pictures taken before and after the reproductive period, they assessed the level of melanin for each individual, male or female, and they also used several traits or data produced such as : stress (as measured by opercular movements frequency), reproductive investment (variation in weight) or reproductive success (number of offspring produced). 

As a side note, measuring darkness (a proxy for melanin) on trout body is not an easy task, First, our pictures were not top of the notch. Second, a fish is most of the time a 3D object, so working on pictures requires some concessions. Third, what is black ? Or what is dark ?

If you want some advices - or warnings -, contact Vincent Roussille, he spent some nights dreaming about it.

 First question : Is melanin coloration stable in time ?

The above graph indicate that the total area covered by melanin on each fish did not really change before and after reproduction: the trait appears to be stable, as it is expected if the genetic basis is strong. Plasticity seems to occur, though. 

Second question: Is melanin coloration correlated with stress ?

Vincent did not find any statistically significant relationship between opercular movements frequency and melanin coloration. It does not fully excludes a possible link, since stress is usually better approached by hormonal concentration measures for instance. Other studies did in fact find some correlations [2].

Third question : Is a greater melanin coloration associated with a greater reproductive investment ?

Here, Vincent found that the darker the robe, the more important the loss of body mass during reproduction, but for males only. This sexual difference rings a bell, because other authors have found that melanin based coloration could be related to aggressive behaviour, a trait that is of major importance in intra-sexual competition in salmonids.This is cool because Vincent also found that males generally presented a more intense melanin coloration than females.

Fourth and last question : if darker males are not stressed, and invest more, do they sire more ?

Hey guys, this is ecology and evolution, and rarely do things go where you expect them to ! So no, we did not find a correlation between robe darkness and reproductive success in males (and neither did we find it in females).

This seems contradictory with published studies, that show that darker males produce offspring with higher survival for instance [3,4] or that they are more competitive to access females through intra-sexual competition. But it only seems contradictory : it takes two to tango, and up to now, nobody said brown trout females were preferring darker males, in which case their superior competitive ability and the good genes they are supposedly carrying may only compensate their lack of attractivity for females.

But hey, that is just a hunch, and we did not yet test it.

I earlier said that Vincent and Lisa were investigating two avenues. The second is a protocol performed directly in natural populations, so we expect new exciting results soon from them ! Meanwhile, Vincent's report can be downloaded here.

References

[1] Jacquin, L., Récapet, C., Bouche, P., Leboucher, G. & Gasparini, J. 2012. Melanin-based coloration reflects alternative strategies to cope  with food limitation in pigeons.  Behavioral Ecology, 23, 907-915.

[2] Kittilsen, S., Schjolden, J., Beitnes-Johansen, I., Shaw, J. C., Pottinger, T. G., Sørensen, C., Braastad, B. O., Bakken, M. & Øverli, Ø. 2009. Melanin-based skin spots reflect stress responsiveness in salmonid fish. Hormones and Behavior, 56, 292-298.

[3] Marie-Orleach, L., Roussel, J. M., Bugeon, J., Tremblay, J., Ombredane, D. & Evanno, G. 2014. Melanin-based coloration of sneaker male Atlantic salmon is linked to viability and emergence timing of their offspring. Biological Journal of the Linnean Society, 111, 126-135.

[4] Wedekind, C., Jacob, A., Evanno, G., Nusslé, S. & Müller, R.  2008. Viability of brown trout embryos positively linked to melanin-based but negatively to carotenoid-based colours of their fathers. Proceedings of the Royal Society B: Biological Sciences, 275, 1737-1744.