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ECOLOGY

Climate for seduction

Temperature and moisture in the environment influence animals’ reproductive strategies

Harvestmen: with spiny legs that they use as a whip, males of the species Serracutisoma proximum fight for territories where females lay their eggs

Bruno A. BuzattoHarvestmen: with spiny legs that they use as a whip, males of the species Serracutisoma proximum fight for territories where females lay their eggsBruno A. Buzatto

Some are brightly colored, larger than the females, brandish “weapons” and defend their territory at all costs; others have discrete coloration, look very much like their partners and waste no time fighting for space—they get directly to the point when it comes time to reproduce. With some variation, these two profiles can be used to explain the sexual behavior of males of various species. Generally speaking (though this does not always reflect reality), the first group inhabits the tropics, and the second lives in temperate regions. What this dichotomy fails to take into account, however, is that regions as dissimilar as the Brazilian Caatinga scrublands and the European Alps—tropical and temperate climates, respectively—have features similar enough to host species with like sexual behaviors. According to a theory posited by researchers including Glauco Machado of the Biosciences Institute at the University of São Paulo (IB-USP), what defines the sexual behavior of species is not only temperature and moisture, but also climate stability—the length of time during which these parameters are ideal for plant and animal activity, and therefore for reproduction.

According to this theory, longer-lasting temperature and moisture conditions favorable to the development of organisms in a region—the so-called reproductive window—give the males more time to fight for access to females, and for the latter to choose their partners, i.e., sexual selection. In the case of the opiliones, or harvestmen, also known as daddy longlegs—arachnids less well-known than spiders and the object of Machado’s study—this high degree of selection is visible in some behaviors displayed by the males while defending their territory. They fight for areas attractive to females, such as those offering water, food or shelter. Such behavior can also be observed in physical traits they exhibit, such as “weapons” (spines on their legs). If the climate is unpredictable, living creatures tend to reproduce in just a few days, because the appropriate temperature and moisture conditions (rainy, but no snow) last so briefly that the reproductive window leaves little room for selection, and the animals are not as flashy or combative.

“There is a simplistic view that the tropics are a homogeneous region, with hot temperatures and plenty of rain throughout the year,” says Machado, who is an expert on harvestmen (see Pesquisa FAPESP Issue nº 144). Another oft-used simplification, he says, defines a temperate climate as anything that is not tropical. Both tropical and temperate regions, however, encompass a wide variety of environmental conditions, such as hot, dry climates in desert areas, and cold, moist climates in the northern forests. Such simplifications do not take into account, for example, that in both the Caatinga and the Alps, the period of time suitable for reproduction, in terms of temperature and moisture, is short, and in some cases it is unpredictable.

In order to test the hypothesis that reproductive strategies vary according to temperature and moisture conditions, a group led by Machado analyzed about 100 harvestman species scattered across five continents, that live under different climate conditions and exhibit a variety of sexual behaviors. In most of these species, the males fight for access to the females under a system known as scramble competition. In this type of competition, males and females become fertile at the same time and go out in search of partners before the weather gets too dry or cold. According to the theory posited by Machado and his colleagues, this strategy would be observed when the reproductive window is so short that there is no time to protect a territory where the female might safely lay her eggs.

The survey, soon to be published in a special volume of American Naturalist, includes data from previously published studies, as well as other data collected by Machado’s team or his collaborators. The researchers tabulated data on behavior and morphology (presence or absence of “weapons” and size of the male compared to the female), and on features of the regions where they live, such as temperature and rainfall. The cross-referenced data corroborated their predictions that climate stability promotes reproductive exuberance. “It’s clear that it is not just sexual selection that molds the species,” Machado explains. “There are other factors such as natural selection, but we proved that the longer the reproductive window, the greater the competition for females,” he says, differentiating the evolutionary force based on selection of partners from the more well-known force in which survival plays the key role in survival and the ability to leave descendants. In the case of harvestmen, the window can last from a month in very cold climates to a year in species that live in tropical forests.

In Rhinella crucifer toads, females (red) are larger than males

Célio HaddadIn Rhinella crucifer toads, females (red) are larger than malesCélio Haddad

Test of strength
One of the group’s objectives is to get other researchers to test the theory with additional species of animals, and even plants. The article on harvestmen is an outgrowth of the book, Sexual selection: Perspectives and models from the Neotropics (Academic Press), published in 2013 and edited by Machado and biologist Regina Macedo of the University of Brasília (UnB), in which an initial version of the idea was introduced. In the year following its publication, ecologists Paulo Enrique Cardoso Peixoto of the State University of Feira de Santana, state of Bahia, and Luis Mendoza-Cuenca of the Michoacan University of San Nicolás de Hidalgo, México, both contributors to the book, tested several hypotheses derived from this theory as part of their research on butterflies. Their findings were later published in Behavioural Processes, in a paper coauthored with Anderson Matos Medina, a doctoral candidate in ecology at the Federal University of Goiás.

With data compiled from 30 butterfly species, they assessed the amount of time the males spent fighting for possession of territories that are visited by females during the reproductive season. The prediction was that, in locations with a long reproductive window, the males would fight more aggressively, while the conflicts would be less intense in areas where the window is short. The predictions were largely confirmed, except for butterflies in intermediate climates, where the reproductive windows last about six months. There, the males invest as little time in aerial battles as those in habitats with an unstable climate, where the reproductive window is short. “This shows that there are other factors at play besides the reproductive window—factors that we can now investigate,” says Peixoto.

Fights between butterflies are tests of strength in which two males fly around one another until one tires and gives up. These clashes were observed in the species Celaenorrhinus approximatus in Costa Rica, and lasted 46 seconds on average. But Lycaena hippothoe, an inhabitant of cold, dry climates in the Alps of northern Italy, cannot afford the luxury of spending time and energy in lengthy aerial battles, and engages in such clashes for only three or four seconds—a notable difference that corroborates what was observed in the harvestmen. “The important thing is that we demonstrated that the theory can be used for other territorial species,” the researcher notes.

Tropical selection
For now, studies employing the new theory—which takes into account more detailed aspects of the variation in climatic factors, and not just the distinction between temperate and tropical climate regions—remain focused on arthropods. The model is applicable in part to tailless amphibians (toads, frogs and tree frogs), according to zoologist Célio Haddad of the Institute of Biosciences at São Paulo State University (Unesp) in Rio Claro. In areas with prolonged moisture, he explains, there are proportionately more territorial species, with a prolonged temporal reproductive pattern and males with larger body size (which increases efficiency when fighting other males). However, he does not believe this type of dimorphism, or others such as color, presence of calluses, spines or an external vocal sac, are more evident in these species.

“On the contrary, environments where there is less rain and moisture generally feature strong size dimorphism. Under these conditions, the females must transport large numbers of oocytes, so they are larger than the males. In addition, the males usually develop calluses on their feet that enable them to stay firmly attached to females and make it difficult for competitors to steal them away,” he explains. In other words, male amphibians do indeed exhibit more territorial defense in moist areas. But sexual dimorphism is also subject to other factors that are also linked to natural selection.

One image, three versions: uakari as seen by the human eye (left), by female uakaris (trichromatic vision) and by male uakaris (dichromatic vision)

Mark Bowler/Proceedings B One image, three versions: uakari as seen by the human eye (left), by female uakaris (trichromatic vision) and by male uakaris (dichromatic vision)Mark Bowler/Proceedings B

Females of vision
Ability to see colors may be linked to both sexual selection and natural selection in the uakari monkey

Its crimson-red, hairless face has earned the bald uakari monkey (Cacajao calvus) the nickname “English” monkey, in an allusion to the sunburned faces of European tourists who forget to use sunblock. For the females of this Amazonian species, however, the shade of red can help them decide whether a male would be a suitable father for their young. It is a tool for sexual selection, although it has not been analyzed in regard to climate. Since these monkeys are subject to diseases such as malaria, which turns them pale, red is an indicator of good health stamped on the face. But not all females are able to see it. “For the first time in this genus we have analyzed a gene known to produce the visual pigment opsin in other primates,” says biologist Josmael Corso, who performed the research during his doctoral studies at the Federal University of Rio Grande do Sul (UFRGS) under geneticists Thales de Freitas and Nelson Fagundes.

Since this gene is on the X chromosome, of which males have only one and females have two, all the males have dichromatic vision (which does not differentiate shades of red), while the females may have two copies of the gene and thus develop trichromatic color vision like that of humans. In the study, published in April 2016 in the journal Proceedings of the Royal Society B, Corso raises the hypothesis that what occurs in the case of the uakari is a balancing selection. The trichromatic vision of some females can be useful in selecting healthy males, but the females that have only one copy of the gene and thus see less color diversity have other advantages.

“Experiments on other primates show that dichromatic vision is advantageous for distinguishing foods of very similar coloration, such as leaves and some fruits,” says Corso. The study concludes that natural selection in these populations is responsible for sustaining both the female monkeys that are skilled at selecting males and those that are good at finding food.

Project
Macroecology of sexual selection: large-scale influence of climate on sexually selected traits (nº 2012/50229-1); Grant Mechanism Regular Research Grant; Principal Investigator Glauco Machado (IB-USP); Investment R$138,988.84.

Scientific articles
MACHADO, G. et al. Macroecology of sexual selection: A predictive conceptual framework for large-scale variation in reproductive traits. American Naturalist. In production.
PEIXOTO, P.E.C. et al. Do territorial butterflies show a macroecological fighting pattern in response to environmental stability? Behavioural Processes. V. 109, p. 14-20. November 2014.

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