This is a picture of a wood duck. It's not the greatest picture in the world but it does make a point. The female (out of sight behind the male) has relatively simple, plain plumage while the male is both brightly colored and has an elaborate pattern. Many of the most striking color patterns in the natural world are ones that occur only in a single sex, and most commonly in males. Follow me below the fold for an exploration of Darwin's other theory: sexual selection.
All images other than the wood duck are from Wikimedia commons.
Darwin first came up with his idea of evolution by natural selection in the late 1830s, some 20 years before publishing the 'Origin of Species'. One reason for the long delay was the knowledge that his idea would be subject to intense criticism and he wished to amass as much evidence as possible to muster a convincing defense.
Several categories of traits (characteristics of organisms) seemed problematic and vulnerable to criticism. Darwin spent considerable space in his book discussing problems for his theory. Many of these problems are the impetus for dynamic research areas in modern evolutionary biology.
One obvious problem was the widespread existence of sexual dimorphism, sex differences in size, color, ornamentation, etc. Some sex differences were not problematic. Differences in reproductive organs (primary sexual characteristics) didn't pose a problem, nor did differences involving secondary sexual characteristics such as mammary glands that were directly involved in having/rearing offspring.
What were problematic were secondary sexual characteristics that had no obvious link to the production of offspring. Let's look at a couple of examples that will be familiar to most people interested in birding in North America. Cardinals are a type of finch, a seed eating bird. Males and females are similar in size and shape but males are bright red in color while females are brown with just a hint of red.
Even more strikingly, red-winged blackbird males and females look so dramatically unlike each other that it would be easy to think them different species. Males are black with bright epaulets on their wings. Females are brown and streaked.
The problem Darwin saw with these characteristics is that if the color of one sex increased the probability of survival, why didn't this coloration occur in both sexes? The bright colors of the males in these cases would seem to make them more conspicuous and vulnerable. The problem becomes even more acute when you consider examples such a peacocks where the elaborate plumage and long tail seem like an obvious handicap to males not getting eaten.
Darwin's explanation may seem obvious to us now, after 150 years of exposure to evolutionary thinking. It certainly wasn't at the time. Darwin proposed that these traits evolved through competition for mates. In other words they evolved because individuals with the traits mated more often and had more offspring than individuals (of the same sex) without the traits. It didn't matter if the traits aided survival of the individual bearing them as long as they resulted in having more offspring.
Darwin further proposed two mechanisms for the process of sexual selection (as he called his second theory): intrasexual selection and intersexual selection. It should be noted that these are modern terms and not ones he used.
Intrasexual selection refers to selection acting within one sex. It is often referred to as male/male competition although this term is now frowned upon for reasons I'll explain in a couple of paragraphs. Traits such as increased size of one sex or weaponry such as the antlers of deer often seem to be related to direct competition among members of one sex for reproductive access to members of the other sex.
Intersexual selection refers to selection mediated by interactions between the sexes. It is frequently called female choice although, again, this is somewhat inaccurate. The idea is that traits such as colors, ornaments (e.g. long tails), songs, etc. have evolved because they are attractive to members of the opposite sex and result in increased matings.
As mentioned above a general observation is that these kinds of traits can be most commonly observed in males. Another general observation is that males commonly compete strongly for access to females and that females are more selective than males in mating. There are good reasons for these general patterns. Eggs are larger than sperm and more energetically expensive to produce. The number of offspring a female can produce is generally limited by her egg production while a male's offspring number is more likely to be limited by the number of females with which he can mate.
The above paragraph is a generalization and the real world is more complicated. There are plenty of 'role-reversed' species such as the phalaropes, shorebirds in which brightly colored females lay eggs in the nests of a 'harem' of males. The intensive study of sexual selection over the last few decades has revealed many subtle interactions that never occurred to Darwin. So the formerly popular terms of male/male competition and female choice have fallen out of favor as they do not adequately convey the complexity of the phenomena.
Darwin published his ideas on sexual selection as a chapter in the 'Origin' and then, just over a decade later, as half of the book 'The Descent of Man and Selection in Relation to Sex' in which he tackled two of the most controversial aspects of evolutionary biology. Sexual selection was controversial, even among some biologists who were strong champions of evolution in general. Alfred Russel Wallace, the co-discoverer of natural selection was one of these. Intrasexual selection was not in question, combat among stags, rams, and other male animals with 'weapons' could be easily observed and related to mating success. What was widely doubted was the existence of intersexual selection. The scientific community was widely skeptical the animals could exhibit a sense of aesthetics, a property of which only humans were thought to be capable.
As an aside, this is an interesting example of cultural biases in science. The idea of human superiority and uniqueness was much more strongly embedded in Victorian society than in our own. Also, it has been argued, that Victorian views of human female sexuality made it difficult for them to imagine females actively choosing mates. For whatever reason mate choice and intersexual selection were largely ignored for a century.
Darwin's idea begs two important questions: is there mate choice based on secondary sexual characteristics and why should mating preferences based on otherwise 'useless' characters exist?
The first of these questions wasn't really studied until the 1960s and it wasn't until the late 1970s and into the 1980s that this field exploded. Mating preferences based on secondary sexual characteristics such as color, song, etc. are now known to be widespread across many animal groups. Testing mating preferences is not as straightforward as one might imagine. You need to control for variation in other characteristics and you need to be sure that the sex with the trait does not influence mate choice in other ways.
The second question - e.g. why do female cardinals prefer to mate with red males? - is the subject of the rest of this diary. The evolution of mating preferences has been a 'hot' topic in evolutionary biology for several decades now. Here are some of the major ideas.
Runaway Selection. This idea was proposed by R.A. Fisher in the 1930s when no one else was interested in the evolution of mate choice. For those of you unfamiliar with Fisher he was probably both the most important evolutionary biologist and most important statistician in the first half of the 20th century. Along with Sewall Wright and JBS Haldane he constructed the mathematical body of theory linking the mechanisms of genetic inheritance to evolution. He also developed analysis of variance and started the whole field of experimental design.
On the other hand he was a eugenicist, a firm believer in the superiority of the British upper classes, and apparently a fairly unpleasant person. (Haldane apparently said at one point that he felt that the task of presenting the mathematical basis of evolutionary genetics to other biologists largely fell to him because Wright was too nice to argue with anyone and no one wanted to deal with Fisher). This is kind of beside the point but I think it is a valuable example of how people can be so brilliant and insightful in one area and so blind in another.
Anyway the idea is that there are genes coding for the trait (say the color red in male cardinals) and other genes coding for the preference for the trait. The trait genes are expressed in one sex and the preference genes in the other sex but all genes occur in both sexes. The process starts out with some variation in the trait in one sex (e.g. in ancestral cardinals males are mostly brown but some males have a small amount of red). Then a mutation arises that leads to a few female cardinals expressing a preference for males with more red color. The females with the preference will mate with the redder males and their offspring will inherit both the preference and color genes.
Males with the color will now have an advantage. Females without the preference are as likely to mate with them as with a random male in the population but females with the preference will mostly mate with red males. So red males will on average have more offspring. Because red males will tend to also have the preference genes both the preference and the trait will spread in the population through positive feedback.
Direct Benefits The least controversial idea about mate choice is if the choosing sex can gain directly by making a good choice. If, for example, the brightness of the male cardinal or the quality of his song provides the female with accurate information about the quality of his territory or his quality as a provider of food for the chicks then choosing bright colored males is a no-brainer.
Good Genes The idea that has provoked the most controversy is that mating preferences have evolved so that members of one sex can choose mates of high genetic quality so that their offspring will inherit those 'good genes'. To return to the cardinal example the brighter the red of the male cardinal, the higher quality genes he would have. A female who mates with a bright red male would be providing her offspring with those same genes.
Sensory Bias The idea here is that the trait has evolved to 'exploit' a pre-existing bias in the sensory system. Imagine that cardinals are particularly sensitive to the color red because an important food source is red. The red color of males has evolved because females were attracted to red for a different reason.
It is important to note that these ideas are not mutually exclusive. Each of them has problems associated with it.
The problem with the runaway hypothesis is that no one has figured out a good way to test it. It explains the origin of traits and preferences and can, based on theory, sweep through a population very quickly. Unless you were really lucky and saw it happening it is very hard to know how important it is.
The sensory bias hypothesis has a similar problem. It relies on some sort of historical reconstruction to be sure that the preference was in place prior to the trait. More detailed studies of neurobiology and sensory systems are really needed to get an idea of the importance of pre-existing sensory biases.
The good genes idea has caused decades of academic debate. The idea as originally proposed, is clearly untenable. If bright colored males have the best genes then those males will get the vast majority the mates and very soon all the individuals in the population will have those best genes. Sexual selection is a very powerful evolutionary force and will quickly remove all genetic variation associated with the trait. There would be no reason for females to choose based on genetic quality in our cardinal example as all the males would have the same 'good genes'.
More sophisticated good genes models have been proposed over the last quarter century or so. All are based on the observation that traits important in mate choice tend to be highly condition dependent, meaning that their expression is more tightly tied to environmental factors than other traits. To use the cardinal example once again - factors such as nutrition during development, recent diet, and illness are going to affect the red color of the male's plumage to a greater degree than those same factors are going to affect wind length. The interpretation then is that the trait (red color in this case) is an indication of mate quality in some general sense rather than being linked to specific quality genes. Because of variation in the environment over time which genes are 'best' will vary.
Studies have tended to focus on fairly simple traits such as the brightness or extent of a single color or the size of a crest or tail. Investigations into the evolution of complex patterns such as you see on the Wood Duck at the top are much more difficult. A lot more will need to be known about the neurobiology underlying preferences and about the developmental biology of the patterns. In other words we have the foundation and framework of our understanding and we need to work on the details of the architecture.
Note: This diary doesn't begin to address the complexities of this field. I've completely ignored the influence of different types of mating systems and patterns of parental care. I've also ignored the interesting examples where both sexes have bright colors and/or elaborate plumage. And, because this is part of the color series, I've ignored non-visual traits completely. Hopefully TexMex will forgive the shamefully neglect of the Orthoptera and other acoustic signaling animals that resulted from this focus. lineatus may note that I have failed to note the reverse size dimorphism in many raptors. Females are dramatically larger than males in many hawks, eagles, and owls. This appears to be one case that is not due to sexual selection but rather selection to maximize the range of prey that a breeding pair can catch to feed their chicks.