Beauty involves so many pivotal and instinctive aspects of life that we might accept it, as is, without defining it or considering its evolution. The topic starts simply enough with such iconic examples as the huge tail on a peacock, the brilliant plumage on birds-of-paradise, and the elegant structures built by bowerbirds. In the Descent of Man, and Selection in Relation to Sex, published in 1871, Darwin posited that these extravagant male displays resulted through selection by female choice [see “Beauty Happens”]. Seventy-eight-years earlier, in 1793, Christian Konrad Sprengel concluded in his book, Das entdeckte Geheimnis der Natur in Bau und der Befruchtung der Blumen (“The Newly Revealed Mystery of Nature in the Structure and Fertilization of Flowers”) that the colors, scents, and shapes of flowers are meant not for our eyes but for bees that are attracted to them and serve to fertilize them. Sprengel’s astonishing discovery languished in obscurity mainly because the eminent and contemporary writer/philosopher/poet Johann Wolfgang Goethe roundly ridiculed this idea of pollination (bees working for the benefit of flowers, and flowers rewarding them with nectar) as a silly intrusion of proximate human reasoning. It would not make sense to human rationality until at least some of the mechanics of evolution by adaptation and survival of the fittest had been worked out, or at least enunciated, and distinctions could be made between proximate and ultimate causation. However, even Darwin, in his original thesis of “survival of the fittest,” could apparently find no reason why the peacock’s long, ponderous tail could make the animal more fit. The opposite seemed true: that it saddled the bearer with a huge cost.

The results of natural selection based on aesthetics may appear neutral or anti-fitness, but that may be so when interpreted proximally, without taking ultimate benefits into account. Consider again the peacock’s monstrous tail and the woodcock’s exuberant sky dance in spring. They are undoubtedly energy-costly and conspicuous to predators. However, investment in these traits is the price these males pay to propagate. Females who initially made the arbitrary, aesthetic choice to select mates with these traits will have offspring that also have these mate preferences and traits, and the investment costs for such displays may escalate with successive generations. It is important to remember that although such selection increases the death-rate of some participants and decreases the reproduction of most, it correspondingly increases the number of young sired by the few that have the trait. Fitness always refers to those that succeed, not to those that fail. It is adaptation of individuals to their environment that is ultimately relevant, and in this case the pertinent environment that males face in mate-selection is competition from others. Therefore, the trait that may kill many males is a fitness marker that females must choose to pass on their genes. And to do that they must be aesthetically attracted to such males.

The issue is not whether an aesthetic signal leads to fitness for the species; it is whether or not it signals fitness for individuals in the species. However, a more profound question is how does the population of many individuals agree/converge on one very specific and seemingly arbitrary model that appeals to all. That this process happens routinely seems at first glance all the more remarkable. In many birds, for example, speciation into very similar sibling species has been driven by aesthetic tastes in mate selection that have diverged most widely, and routinely.

The problem is old. Throughout ice ages and interglacial intervals, ocean levels fell and rose; forests spread over the globe and then shrank to remnants on mountain tops. Likewise, other plant and animal populations increased and spread widely, then shrank to small remnants. Species evolved into sister species in these isolated, evolving eco-environments. These separated island habitats later reconnected when climates changed, and isolated populations reconnected. If species had differentiated too far, breeding with each other might have been an unprofitable investment, because they had adapted new or different ways of living. And that is where sexual selection would have been operative. It became important for mate choice to make careful distinctions.

The arbitrariness of the mating signal disappears in this ecological context, the area where previously isolated species reconnect. Differences become adaptive. As in the evolution of habitat preference, where divergence reduces competition, sexual-signal diversion implies selection for occupying different signaling niches. Divergence is the clue to what aesthetics are and why they are adaptive. I posit that the answer is about speciation. Consider two well-known closely related equids, the donkey and the horse. A female horse can mate with a male donkey, but their offspring, a mule, is sterile. In adaptive-evolutionary terms, it behooves a female horse to not squander a mating possibility with a close species when her potential offspring will never pass on her genes. Such cross mating would be especially devastating to monogamous, or short-lived, species such as birds that may only live to breed one or a few times.

Often, species may be highly variable within their species. To be a successful breeder in the face of variance of appearance—which naturally arises in separated populations—an animal must be able to detect a species-defining marker out of the mix of many potential signals. As a young, amateur ornithologist, examining bird specimens in the Berlin Museum fur Naturkunde that my father had collected in the 1930s in Celebes (now Sulawesi), I saw clear differences in at least one species of thrush, Heinrichia calligyna, that had been described by Erwin Stresemann, an eminent ornithologist at the time. Birds from one mountain versus another showed distinct size and color differences, but I could not say if they were the same or different species. Even trained taxonomists have trouble doing that, and Stresemann had not done so. So how could birds do it?  The possible answer came to me thirty years ago in Maine during my field studies of the foraging behavior of bumblebees.

Consider bumblebees as pseudosexual organs of plants. A species blooming at the same time and place as other plant species can only induce pollinators to be flower-faithful by differentiating its flower signals from that of its neighbors. Suppose competing plants had a simple platform flower that is colored red. If the bees saw the flowers of the two plant species as the same, the plants would be “mated” indiscriminately. The more that flowers of two adjacent species differ from each other, the greater probability that bees will be flower-faithful, and thus make more plant visits and raise the chances for fertilized seed, and offspring. The signal, as such, is arbitrary only if there is no competition, which is hardly ever the case.

The reproductive biology of plants has close parallels to that of animals, and the contrasts illuminate our understanding of their biology. Flowers that serve as aesthetic attention-getting ornaments evolved from leaves. All around the deep woods by my cabin in Maine, for example, some of the petals of bunchberry dogwood (Cornus canadensis) and hobblebush (Viburnum lantanoides) start out pale green as pseudo-leaves before they expand to become white and attention-getting. They are arranged in inflorescences where outer flowers are for show, lacking ovaries. Wheth-er as individuals or as inflorescences, flower forms that serve as aesthetic attractants also have signposts and alleys and guardrails that physically guide pollinators to their reproduc-tive organs; aesthetic and utilitarian functions merge.

With two very similar bird species living in close proximity, the same selection principles apply. The key issues are: signaling to draw attention, maintaining fidelity to that signal; and having that signal stand out by a difference—preferably, a huge difference—from the competing signals. In birds, courting features can be both visual and acoustic; in rodents, dogs, and insects it can be scent. Aesthetic symbols of beauty will in time diverge by natural selection based on fitness.
And in many insects (and among primates), there are differences in genitalia morphology that prohibit or discourage mating among different species, even if they try.

Animal-pollinated plants have numerous ovaries, with each adorned with specific allures. These attracting ornaments usually shrivel and drop off within days or hours after ovaries are fertilized. Retaining aesthetic ornaments on fertilized ovaries dilutes visitation to those not-yet fertilized. Bird sexual allurements can also attract predators. Although birds cannot shed their ornaments on short notice, because feathers have other functions, they can reserve their conspicuous showing to specific, short time periods.

It is important to note that fitness is, or can be, a composite—in varying proportions over time and place—of selection for signaling and for other functions. For example, flower petals evolved from leaves that gradually lost chlorophyll, thus showing sunscreen pigments. The various-colored petals increasingly took on a signaling function. However, some flowers, such as bunchberry that grow in shady woods, have both show and photosynthetic functions; they have some chlorophyll to capture solar energy when they first open, then after several days they lose their minor leaf function and become fully white, which attracts pollinators. In the hobblebush, which grows next to bunchberry, outer flowers of the inflorescence are large and white. They have no reproductive parts. They are for show to lead pollinators to the small inner flowers that have anthers, pistils, and ovaries. Only the latter flowers perform the reproductive function of generating seeds. Apparently, adaptive features are multiple and can be allocated simultaneously with aesthetic function aimed at mating partners, or independent of them. They act together to accomplish the same thing—reproduction.

Humans are the best example of rapid changes in aesthetics, and with the same object of mate choice. We have signals for sexual preferences (e.g., body shapes) that may have been derived—as the green leaves to flowers scenario—directly from utilitarian individual fitness. But they are now arbitrary and confer no survival benefits.

Signals are no more, nor less, than the adaptive attractions of a species to particular songs or dances. They evolved for fitness, derived from discriminating aesthetic senses of beauty. But an important point of note is that change happens, especially, in humans. Fitness may be no more than the ability “to be glib at sixteen,” as one of my professors once quipped. But consider the changing of styles, from time to time and from culture to culture: body types, grooming styles, cosmetics, fragrances, body adornment, body art, clothing. Worldwide, we have a wide variety of displays that change frequently. Perhaps similarly, male humpback whales advertise themselves by their unearthly and haunt-ing songs. All those within hearing range sing the same complex song, but these songs change over the years, and all the whales adopt the new song. This pattern suggests an inherent love of novelty, or neophilia, an aesthetic for the new, which I documented in young ravens as an adaptation for finding new food. Ravens, unlike most animals, are not hard-wired to feed on any specific berry, insect, or thing. Instead, they rely on intelligence, and after leaving the nest they examine and pick at all novel items they encounter, to then quickly learn to ignore all that are not food. But in the process, they are then able to feed on whatever the environment has to offer. As a result of this aesthetic, they can and do live in the widest habitat range of any animal, matching our own.

What attracts is what conforms and then defines a norm. When all are alike, the unique stands out, and that which adds a little something draws attention. It is what is looked at, heard, and noticed from out of the lineup. And once it is chosen, it is passed on. (culturally, in the case of humans and whales). It becomes adaptive and continues to evolve. But there are bounds within each environment and genetically with each species. Although humans are of the primate order, their displays won’t evolve to have bright red and blue faces like male Mandrill baboons or blue genitalia as have male vervet monkeys.

Likewise, a specific adaptive sexual attraction within a species can function as a warning signal to other species. Indeed, it is precisely the conspicuous eye-catching displays (of colors as well as scents and sometimes sounds) of many insects that deter predators. With beetles, such as leaf beetles and lady bird beetles, predators learn to associate color patterns and/or scent with noxious secretions and toxins that their potential prey has manufactured or incorporated into their bodies from ingestion of certain food plants.

We are beginning to understand the role and evolution of animal aesthetics. Humans do not necessarily have their own dynamic, but some of our evolving aesthetics involve learning that often dictates mate choice, habitat choice, food choice, entertainment, and art.                                                    --BH