This diary is super long. However I have structured it so you can skip a big chunk in the middle if you just want the intro and cool bird displays.
One of the iconic images of the tropics is of brightly colored birds flitting through the vegetation. This is a bit misleading, although there are plenty of brightly colored birds in tropical forests. However, detailed studies have shown that birds in the tropics are not, on average, more prone to bright colors than temperate birds. There are just a lot more species overall in the tropics and thus more colorful ones. Among the colorful species there is variation. In many species such as most parrots including the scarlet macaws above both males and females are similarly brightly colored. This is very common in tropical forests. However, this diary is focused on species where the sexes are very different in appearance. What we are discussing are extreme examples of sexual selection in some tropical forest birds. These birds are justly famous for their extraordinary plumage, calls, and visual displays.
Short Inset on Sexual Selection: You don’t have to read this section to get the gist of this diary. But if you are unfamiliar with ideas about sexual selection it might be worth your while to read the next three paragraphs. Or if you are really keen you can read the longer section on mate choice but that isn’t necessary for the part that is actually about birds. If you are feeling really confident or annoyed with all my excess verbiage you can just skip down to the birds.
Charles Darwin proposed the idea of sexual selection in a chapter of the ‘Origin’ and gave a more expansive treatment of the subject in half of a book (The Descent of Man and Selection in Relation to Sex) in 1871 (the other half of the book is concerned with human evolution). Sexual selection was used to explain characteristics that Darwin otherwise considered problematic for his theory of evolution by natural selection. The characteristics in question were ones that differed between the sexes of a species and were not directly involved in reproduction. Examples would include size, color, or behavioral differences between the sexes as well as ornamentation such crests or tails that differed between males and females. Many of these traits seemed to place the bearers at a disadvantage for survival and, if they were advantageous, why weren’t they found in both sexes?
Darwin proposed that these traits evolved because they aided in competition for mates. He identified two ways this could happen. In intrasexual selection members of one sex directly compete with one another for access to mates. Generally, although by no means universally, males are the competing sex. Traits that aid in this competition (e.g. antlers in deer, elaborate antennae for detecting female pheromones in insects, large male size in elephant seals) can evolve because they allow individuals to directly outcompete members of their own sex.
In intersexual selection the competition is more indirect. One sex (generally but not always females) chooses mates using traits in the other sex (colors, calls, ornaments, etc) as the basis for their choice. The traits in the other sex evolve as a result of selection exerted through mate choice. In other words, traits such as long tails evolve because males with those traits are chosen as mates more often. Darwin framed mate choice in the context of an aesthetic sense in females.
Mate Choice (an evolutionary puzzle):These two ideas were received very differently by the scientific community of the time for a variety of reasons. Intrasexual selection was accepted by natural historians (at least those who accepted Darwin’s other ideas) and the idea of traits evolving due to selection driven by direct competition for mates has been non-controversial ever since. However intersexual selection was not accepted by Darwin’s contemporaries and, in fact was not a mainstream idea in evolutionary biology until about a century after it was first proposed by Darwin in the ‘Origin’.
So why was intersexual selection (evolution of secondary sexual characteristics driven by mate choice) controversial? One reason is that Darwin’s idea of animals having an aesthetic sense was seen as an outlandish notion by Victorians. The idea of females actively choosing their mates also went against the Victorian notion of women as being passive and not interested in sex. It is important to note that an aesthetic sense is not necessary for mate choice – members of the choosing sex only need to be attracted to particular stimuli. In fact, neither of these objections has been seen as serious obstacle to sexual selection by mate choice for many, many decades.
The real puzzle is, why do individuals use these apparently arbitrary characteristics to choose mates? What does a peahen gain from choosing to mate with a peacock with particularly bright plumage or a particularly long tail? The answer has never been obvious and, lacking any kind of functional/adaptive hypothesis the idea of mate choice languished until the 1960s. At this point, empirical evidence that females1 in many species were actually choosing mates based on traits like tail length began to accumulate and evolutionary biologists belatedly realized they had an intriguing phenomenon that required explanation.
1.To reduce the complexity of the writing I’m going to switch to talking about female choice for male traits exclusively at this point but bear in mind that the reverse may be going on in some species.
Sexual selection by mate choice has been a ‘hot topic’ in evolutionary biology for many decades now. A plethora of hypotheses have been proposed for the evolution of mating preferences and thus the traits themselves. All of them have strengths and problems and the hypotheses are not mutually exclusive. I’ll briefly discuss four of them that are both popular and relevant to the examples in this diary. The first two are adaptive explanations (i.e. female fitness is positively affected by choice) and the other two are non-adaptive explanations (there isn’t necessary a benefit to females from being choosy).
1. Direct Benefits– This is the least controversial in the sense that in applicable situations everyone agrees it will work. The idea is that females are using male traits as cues that will directly help them have offspring. A male cardinal that is particularly brightly colored may be a better provider of food to the fledglings or a male red-winged blackbird with a loud call may have better territory with more resources for nesting and chick rearing. The problem is that many of the most extreme examples of male traits are found in bird species where the male contributes nothing to producing offspring other than sperm. In these species males do not help care for the young or defend territories in which females nest. Which leads us to our second hypothesis.
2. Good Genes– Based on conversations with students over the years this seems to be the most ‘obvious’ explanation. Even if males don’t provide any direct assistance females can benefit if they mate with males that have versions of genes that confer high fitness (e.g. make individuals more vigorous, healthier, long-lived, etc. than average). These ‘good genes’ would then get passed on to the females’ offspring, increasing their chances of being successful. This idea is intuitively appealing but it has a major flaw when you attempt to demonstrate it with a mathematical/genetical model.
The problem is that both natural and sexual selection will favor the increase of the ‘good genes’ in the population. Sexual selection on males can be a particularly powerful force because of the very large number of offspring a single male can have. In extreme types of mating systems, it is not unusual for maybe only 5% of males to sire 90% of the offspring. As a result, these good genes should increase in frequency very rapidly until they are only the versions of those genes left. At which point there is no longer a benefit to making a choice.
More sophisticated models of good genes processes invoke the idea that male traits are highly condition-dependent. In other words, their expression depends very highly on the health and vigor of the individual. Thus, they aren’t linked to particular genes. As the environment changes, different genes will be favored.
3. Runaway Sexual Selection. This idea is older than the others. It was first proposed by pioneering evolutionary geneticist R.A. Fisher in a verbal model published in the late 1920s. Mathematical models were developed in the 1980s. Basically, the idea is that the genes for the male trait and the female preference for the trait arise independently in a population through mutation. Both sexes can have both genes but the trait gene is only expressed in males and the preference gene is only expressed in females. Females with the preference gene will tend to mate with males with the trait gene and thus the two genes will rapidly come to occur in the same individuals and get passed on together. Males with the trait will have an advantage (they get all the matings from females with the preference as well as a proportional share of matings from females without the preference) and thus both the trait and the preference will increase in the population through positive feedback.
This model is very appealing to geneticists because it is elegant and it explains the evolution of the preference without having to worry about how it might benefit the female. The main problem with this idea is that, at best, it is extraordinarily difficult to test, and might well be, for all practical purposes, untestable. The runaway process is thought to stop once natural selection against the trait counterbalances the mate choice for the trait. The models show that traits and preferences can evolve very quickly in a runaway process. Thus, we are unlikely to see it happening unless we happened on a population at just the right time. All we can see is the end result, a preference and a trait. Another issue is that in order for the process to work, the female preference itself, has to have little or no effect on fitness so that it can be dragged to high frequency by the success of the male trait.
4. Sensory Bias– This is the most recent of the four main ideas to be formally proposed although its roots are in classical ideas in animal behavior that date back to the mid-20thcentury. The idea here is that female sensory/nervous systems have built in biases that evolved for other reasons which are then ‘exploited’ by males. For example, male guppies have orange coloration which is attractive to females. This coloration is similar to the color of a kind of fruit that falls into the nutrient poor streams in which guppies live. Guppies are attracted to this fruit as a source of food. Male coloration is hypothesized to have evolved because females were already attracted to orange.
A Side Note on The Evolution of Beauty by Richard Prum. I’m including this here as it was a comment about this book that partly prompted me to write this diary. As I haven’t read the book myself (I have read several detailed reviews) and as I want to get to the birds I won’t say much. This book is about the evolution of male traits and female preferences in birds. It seems to have had very different receptions from non-scientific and scientific audiences. It was named one of the best books of the year by the New York Times and was nominated for a Pulitzer prize. However, experts on evolution, while recognizing its many values, point out a series of fairly serious problems with Prum’s central thesis.
1. Prum’s definition of sexual selection is much more restrictive than that used by virtually anyone else.
2. Along the same lines, Prum ignores the complexity of sexual selection hypotheses and the fact that they are not mutually exclusive so more than one could be in play in a particular situation.
3. Prum seems to think that the runaway process should be the null model and accepted unless there is evidence for an alternative explanation. Given the difficulty in testing the runaway model this doesn’t seem very scientific.
4. Prum equates the good genes hypothesis with eugenics and thus falls victim to the naturalistic fallacy (see appendix for more detail). According to the reviews, he basically argues that we should prefer a runaway ex planation to a good genes mechanism because it is ideologically more desirable. However science is supposed to be about figuring out what is true rather than what we want to be true.
You can read more about evolutionary biologists response to this book here and here.
Sexual Selection in Birds (at last!). Many birds show differences in color, ornamentation, and behavior between males and females. The most common mating system in birds is social monogamy in which birds pair up and rear young together as social mates. This would seem to reduce the scope for sexual selection as birds would be limited to a single mate each. However, DNA studies have revealed that mating outside of social pairs (i.e. cheating) is quite common. Also males that have attractive traits may attract high quality females or get females earlier in the breeding season and thus sire more offspring.
However, sexual selection is at its most powerful in species where there is little or no social bond between parents and thus males have the opportunity to mate with many females. In birds, the best example of this is in the Galliform birds: chickens, pheasants, grouse, turkeys, etc. These birds have highly precocial young which are partly independent shortly after hatching. Males are not needed to care for the offspring and often do not form social bonds with females. This group is noted for elaborate male ornamentation (e.g. turkeys, peafowl, pheasants, sage grouse). Many of these birds have a mating system that involve leks. Leks are collections of mini-territories in which each male only defends a space which is used for displaying to visiting females. In a classic lek all of these mini territories are clumped together. In an exploded lek (as occurs for example in turkeys) the mini territories are scattered through out the habitat. In a lekking system females visit males, observe displays, make a decision, and mate. Males contribute nothing to reproduction other than sperm.
Evolution in the Tropics (more birds!): So how does all this relate to tropical birds? Well there is this persistent notion that evolution in tropical parts of the world is different than in the temperate zone as described by Theodosius Dobzhansky below.
Now, the processes of natural selection which arise from encounters between living things and physical forces in their environment are different from those which stem from competition within a complex community of organisms. The struggle for existence in habitats in which harsh physical conditions are the limiting factors is likely to have a rather passive character as far as the organism is concerned. Physical factors, such as excessive cold or drought, often destroy great masses of living beings, the destruction being largely fortuitous with respect to the individual traits of the victims and the survivors, except for traits directly involved in resistance to the particular factors. As pointed out by Schmalhausen, indiscriminate destruction is countered chiefly by development of increased fertility and acceleration of development and reproduction, and does not lead to important evolutionary advances. Physically harsh environments, such as arctic tundras or high alpine zones of mountain ranges, are inhabited by few species of organisms. The success of these species in colonizing such environments is due simply to the ability to withstand low temperatures or to develop and reproduce during the short growing season.
Where physical conditions are easy, interrelationships between competing and symbiotic species become the paramount adaptive problem. The fact that physically mild environments are as a rule inhabited by many species makes these interrelationships very complex. This is probably the case in most tropical communities. The effectiveness of natural selection is by no means proportional to the severity of the struggle for existence, as has so often been implied, especially by some early Darwinists. On the contrary, selection is most effective when, instead of more or less random destruction of masses of organisms, the survival and elimination acquire a differential character. Individuals that survive and reproduce are mostly those that possess combinations of [[p. 221]] traits which make them attuned to the manifold reciprocal dependences in the organic community. Natural selection becomes a creative process which may lead to emergence of new modes of life and of more advanced types of organization.
What T.D. is hypothesizing, in a rather verbose manner, is that natural selection in temperate regions is driven largely by climate while natural selection in tropical regions is largely driven by interactions with other species. In other words, in the tropics it is always summer time and the living (at least if you don’t get eaten by an ocelot) is always easy.
Birds in tropical regions have small clutches of eggs and long lives. The small clutches are thought to be the result of very high rates of nest predation. The long lifespan reflects the fairly low risk of mortality after fledging (no dangerous migrations or winters).. For a tropical forest bird, each nest is a long shot gamble but with relatively little at stake. It’s likely that her nest of eggs or chicks will get eaten by a snake but there are plenty more opportunities to try. In contrast, a temperate bird has more at stake each time but maybe a better shot at success.
One type of bird is thought to be living on easy street. Frugivory (fruit eating) is a common diet in tropical birds (and other tropical animals such as monkeys). Although many temperate birds certainly eat fruit there are relatively few that are specialist frugivores (cedar waxwings and phainopeplas are the twp examples that some to mind). Winter means little or no fruit is available and temperate birds need other sources of food. In contrast, tropical forests are full of frugivorous birds.
Frugivory seems to be a fairly easy way to make a living. Plants are growing food which has evolved to be eaten for the purposes of seed dispersal. Eating fruit requires mobility to get from one tree to another but isn’t a problem for birds. A lot of the really brightly colored tropical birds are frugivores. Cotingas and manikins in the new world tropics, birds of paradise in New Guinea are the most spectacular examples. In addition to the bright colors and long tails there are also the wild displays you see below and even the structures built by bowerbirds.
Lance-tailed manikin males doing a cooperative display to a female. This is an example of an exploded lek system where males defend these dance perches that are spread throughout the forest. This footage was taken in May 2019 in western Panama in the same location as my field course. Which is why I put it first.
A different manikin. This one breeds at the field station where I taught courses in Ecuador. Unlike the lance-tailed manikins I never saw any of these birds.
Umbrella birds are probably the most spectacular of cotingas.
Although the cock of the rock (shown here in a lek) might be viable contender.
There is speculation that frugivory has reduced natural selection acting on both male traits and female choosiness. Females don’t need males to help rear offspring which results in strong sexual selection on male traits because males can potentially mate with many females. The abundance of food means that males can devote a lot of time and energy doing crazy things to attract mates. Also, although fruit is abundant, the location of fruit in the forest is highly variable in time and space. Therefore it is not practical for males to defend fruiting trees or to defend females as neither is going to occur in predictable locations. Fruits can also provide birds with chemicals that can enhance their color (I don’t know if this has been demonstrated in any of these birds).
Some bowerbirds, like this species, are quite drab in color. The display is actually external to the animal!
A different and more personally spectacular bowerbird species
And a few birds of paradise to complete the diary.
Thus it is entirely possible that the wild coloration, crazy displays, and space vocalizations of the most spectacular tropical birds are the results of eating fruit.
Appendix: The Naturalistic Fallacy. Basically, the NF is the idea that we should look to nature for moral guidance. It is a fallacy, because animal behavior is incredibly variable and one could support almost any action imaginable using an example of something that actually happens in nature. As it turns out nature is full of animals doing things, that if they were done by a human, we would consider horrifying. Examples include traumatic insemination in bed bugs, infanticide in langurs and lions, siblicide in many birds, prenatal cannibalism in sharks, and sexual cannibalism in spiders and mantids.
This is not to say that our own cultural biases don’t affect our interpretation of the natural world. Much as we would like to think otherwise, they obviously do. This is why having scientists with a diversity of backgrounds is very important. Female researchers are probably more likely to pay attention to female behavior in their subjects than male researchers. LGBT researchers are probably more likely to notice and assign importance to same sex directed behaviors.