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From branch to branch

Natural selection aided diversification by size and generated a variety of monkeys in Latin America

MIGUEL BOYAYANSpider monkey: for the largest Brazilian monkey leaves are a veritable banquetMIGUEL BOYAYAN

Looking up in a tropical forest may be just as frustrating as it is amazing. The tops of the trees are home to colors, shapes, sounds and lives of every type; lives that sometimes flash before our eyes, sometimes intrude on our ears and sometimes hide. In the middle of everything the leaves hide in the Americas,  there are some 130 species of monkeys rarely seen by curious visitors. Capuchin monkeys hang by their tails and with them they can also handle the insects and fruit that comprise their diet, which includes a wide range of tasty snacks, such as leaves, flowers, small vertebrates and the bark of indigestible trees such as the eucalyptus or the pine. These monkeys that live in bands of up to 35 individuals usually defend their territory, but curiously allow a smaller species, the black squirrel monkey, which vie for the same fruits and insects, to share branches with them. “It’s as if the black squirrel monkeys were the offspring of the capuchins”, explains Gabriel Marroig, a biologist from the University of São Paulo (USP). He analyzed the variety of monkeys that inhabit the trees in the Americas and concluded that among the characteristics favored by natural selection, such as physical strength and reproductive capacity, the one that counts for most is the animal’s size.

In a recent article in BMC Evolutionary Biology, Marroig compares the proportions of the skulls of capuchin monkeys, of the genus Cebus, and black squirrel monkeys (Saimiri) throughout their growth. They are two related genera of very different sizes, which sets them apart from other New World monkeys. Skulls are the body parts most used in zoology as a source of information because the distances between points of reference, such as depressions, orifices and junctions between bones allow for species characterization and a comparison of different animals. In the hands of the biologist they help to tell what has happened since the monkeys arrived in the Americas 30 million years ago.

The team from the Mammal Evolution laboratory at USP transforms the measurements into three-dimensional images of the skulls analyzed, a technique known as geometric morphometry. With the skull supported on a platform, the researcher touches the points of reference with something that looks like a metal pen hanging from an articulated arm. The movements of this arm, which is linked to a computer, are stored as three-dimensional distances. The computer then generates images that are reminiscent of cut crystal, but that are a simplified version of the measured skulls. Then the researchers can shrink or expand the digital skulls so that the capuchin monkey and the black squirrel monkey are the same size – the former is in fact two or three times bigger than the latter. Thus, they can ignore size differences and compare the proportions between the measurements and the shape of the skull in animals of various ages.

The digital images show that the black squirrel monkey is born with an almost round skull. As it grows its skull gets flatter, as if something pressed the crown of the head down, while the muzzle elongates. Marroig showed that, ignoring size differences, the skull of an adult black squirrel monkey is very similar to that of a young capuchin monkey, which goes through the same process of flattening in one direction and lengthening in another.

Precocious adults
This pattern of diversification fits in with the theory that describes evolution, which can give rise to new species as a result of the changes in the rates of development of an organism. This evolutionary mechanism, known as heterochrony, was for a long time considered a possible explanation of how human beings evolved: it is as if the fetus of the chimpanzee had become an adult without losing its infant appearance. According to Marroig, this hypothesis is no longer accepted. “Differentiation in the human species is more complex, involving many other characteristics over and above rates of development”, he says.

Despite no longer being seen as central for differentiating man from his primate relatives, development continues to be quoted as an important evolutionary force. “There is evidence that alterations in development occurred at significant points in time in the evolutionary history of various groups”, says biologist Tiana Kohlsdorf, from the USP campus in Ribeirão Preto. When it is impossible to find embryos to analyze the action of genes throughout development, Tiana explains that the way to go about this is to analyze the DNA sequences of the genes related to development of the characteristic in question. In her work she compares the genes that work in the formation of feet in lizards and snakes.

Eduardo CesarBlack squirrel monkeys share trees and food with capuchin monkeysEduardo Cesar

In the case of the differences between the monkeys of the Americas, the target of the genetic analyses has been the growth hormone. During her doctorate, when her tutor was Marroig, Elytânia Menezes deciphered the gene that directs the synthesis of this hormone and found evidence of adaptive evolution – variations in the action of the growth hormone between genera might have been caused by natural selection and might be responsible for the  differences in size among the monkeys of these genera. Elytânia plans to present her doctoral thesis at the beginning 2008 and is preparing the paper for publication. We need to wait, therefore, for further details.

Marroig compared aspects of the development of all 16 genera of monkey of the Americas. Concerning size, he found that capuchin monkeys take longer than might be expected to reach reproductive age, which gives them more time to get bigger. The black squirrel monkeys, on the other hand, are born bigger relative to the size of the mother found among other monkeys. “They are born with big heads, and with a more developed brain than other species”, relates Marroig. It is in part thanks to this that they are weaned faster than other monkeys of similar size.

This correlation reinforces the idea that alterations in size are what produced the different genera. The work does not allow scientists to say with any degree of certainty what the common ancestor of the Cebus and Saimiri genera was like. Marroig thinks it is likely, however, that the capuchin monkey is a “grown-up” version of the black squirrel monkey, and not the opposite. This is more than a mere hunch. The longer time that Cebus takes to reach maturity is a clue. Another is the genealogical tree of this continent’s monkeys: the branch where these two genera are located only has small primates.

Fossils and genetic studies indicate that 30 million years ago, in the Oligocene geological period, the first primates reached the New World. “At this time”, Marroig explains, “peninsulas linked Africa to South America”. They were not full bridges between the two continents, but the distances were sufficiently short for the ancestors of the primates that live here today to be able to cross them on tree trunks or other floating material. The map of the bottom of the Atlantic ocean millions of years ago was prepared by Felipe Bandoni, a doctoral student of Marroig’s, for the book “South American Primates“, currently in the press at the Editora Springer publishing house.

These simian immigrants, which were animals weighing around 1 kg (such as black squirrel monkeys, which are 40 cm tall), found a land full of possibilities. “They had no competitors; marsupials were the only other mammals living in trees to some extent, but they used resources differently”, says Marroig. The trees were an “open-house”, with food for all tastes. Then between 16 and 20 million years ago something happened that the evolutionists call adaptive explosive radiation: the sudden appearance of a great variety of monkeys capable of exploiting the most diverse of ecological niches, as defined by their diets.

This is when size enters as the fundamental driver of evolution, because this is what allows for nourishment specialization. “There’s no large monkey that feeds on insects and no small one that survives on the basis of leaves”, says Marroig. This occurs because small mammals need nutrients that can be quickly changed into energy, which they get from fruit and insects. To survive on a diet of this type, larger animals would need to eat a very large quantity of insects. “To do so”, explains the biologist, “they would have to specialize in social insects that can be found in great density, such as the ant-eaters do, or become effective predators”. No South American monkey has developed these characteristics. But eating leaves is not so easy either: they are full of indigestible substances and therefore can only be eliminated by animals with long intestines, capable of extracting nutrients and neutralizing the toxins with which plants defend themselves from herbivores.

Members of the Cebus and Saimiri genera have similar diets, above all fruit and insects. The difference is in the capuchin monkeys’ capacity to complete their diet with almost anything that appears in front of them and in the proportions that they represent. Insects form 50% of the diet of Cebus, monkeys that weigh from 2 to 3 kg and as much as 75% of what the Saimiri eat, the adults of which weigh around 1 kg.

Eduardo CesarThe capuchin monkey is a larger version of the black squirrel monkeyEduardo Cesar

The course of evolution
It comes as no surprise that variation in size is the diversification path of monkeys. “But no one talks about this”, says Marroig. It is foreseeable because natural selection acts on genetic diversity (if a gene is always identical there is no possibility of evolution) and size is a characteristic marked by enormous variability (you only have to run your eyes over a room full of people to get some idea of how size varies). In an article published in 2005 in the journal Evolution, Marroig analyzed all 16 genera of monkey on the American continent and showed that, in the jargon of evolution, size is the path of least evolutionary resistance; in other words, this is the road that evolution tends to take.

Such size diversity may have arisen by chance, or by hitching a ride on the back of other characteristics, such as larger teeth or longer tails. But in an article published in 2004 in the journal The American Naturalist Marroig showed that in most American monkeys it was natural selection and not chance that generated this diversity. “Today we have statistical tools to distinguish which characteristics selection acted on”, explains the biologist.

The most recent count says that there are 129 monkey species in the Americas, with sizes that range from the 100 grams of the pygmy marmoset (Cebuella pygmaea) to the 10 kg of the spider monkeys (Brachyteles arachnoides and B. Hypoxanthus). All of them eat fruit, an easy source of sugar, and adopt different life strategies to complete their diet with proteins and vitamins. The spider monkey frequents the tops of trees in the Atlantic Seaboard Rain Forest, where it gorges itself on leaves. Lower down  the capuchin monkeys  live and lower still the black squirrel monkeys, with their varied diets. In the stratum closest to the ground live the small marmosets that weigh around 400 grams and have long narrow incisors with which they bite into tree trunks to feast on the sap. They also eat fruit, insects and nectar.

Compared to their American cousins, the more than 150 monkey species from the Old World show little diversity in terms of shape, size or behavior. In part they owe this to their more recent diversification. Although the Old World has more species than the New, Marroig argues that it is impossible to compare numbers, and not just because they have separate evolutionary histories. According to the biologist, scientific schools are very different and result in different strategies for classifying animals. “In Brazil the researchers describe new species more easily than in the Old World, where the specialists are more conservative and tend to classify varieties that they come across as sub-species, instead of a species.”

In order to understand in more detail what has happened throughout the evolution of our monkeys it would be necessary to go down the path of development analyses, such as the ones Tiana uses to reveal the evolution of the absence of feet in snakes, in order to check how alterations in growth may give rise such diversity. But until a development expert appears who is interested in going into what Marroig has already discovered about capuchin and black squirrel monkeys in greater depth, the biologist is satisfied and moving on to look for new challenges – other animals and other continents. Members of his laboratory are collecting data about other groups of mammals in order to carry out analyses similar to those that helped tell the story of the monkeys. Marroig is betting that the importance of size for evolution is generalized and he intends to show this over the coming years.

The Project
Morphological evolution, biogeography and systematics in neotropical mammals (nº 04/10346-2); Modality: Jovem Pesquisador and Research Grant – Regular; Coordinator: Gabriel Marroig Zambonato – IB/USP; Investment: R$ 170.487,26 and 65.124,88