It would seem that almost every possible mating arrangement exists in the animal kingdom, from lions with their prides and ants with their colonies, to cheating birds and monogamous voles. But new research reveals that social animals have only two basic options when it comes to reproduction. They can be monogynous like ants, with only one female who mates; or they can be polygynous like chimps, with many females who mate. Depending on which evolutionary trajectory the animals follow, their population size will either grow into the millions or remain relatively small.

How many breeders?

A group of zoologists writes about this finding in a new paper published in Royal Society Open Science. It analyzed 293 different social species, including reptiles, birds, insects, and mammals, and asked two simple questions about each one: how many females live in each group of these animals, and how many of those females are "breeders" capable of reproduction? Study co-author Eileen Lacey, a biologist at University of California-Berkeley, told Ars by phone that it was surprisingly hard to find this data. "In all the studies of social animals, very few people reported critical information, like how many individuals are breeding versus not," she said. Nevertheless, she and her colleagues gathered enough data to perform a statistical analysis of the relationship between number of breeders and female population size.

"The proportion of breeders in societies with more than one reproductive female appeared to be dependent upon the total number of females in the group; when societies with multiple breeding females from all taxa (ants, wasps, mammals, birds) were pooled, we found that the proportion of breeders decreased significantly with the total number of females in the group," the researchers wrote in their paper.

In other words, the fewer breeders there are, the more females in a given social group. There are extreme examples of this in ant and bee societies, where monogynous colonies may contain up to several million sterile females with one fertile queen. A small number of males are produced only for mating seasons, and queens mate just once (though possibly with more than one male). On the other end of the spectrum are polygynous animals like birds and primates, where every female in the group is fertile, but females make up only about half the population. For this study, the term polygynous refers to any social group where more than one female is fertile and reproduces. It does not refer to "harems," where one male has multiple female mates, though some polygynous animals like lions do form groups where a male mates with multiple females.

This finding caps off a longstanding debate within zoology over whether mating strategies fall on a continuum of infinite options or cluster around just a few possible ways to organize reproduction in social groups. Lacey and her co-author Dustin Rubenstein, a biologist at Columbia University, originally believed that they would find a continuum. Indeed, Lacey was an author on an influential paper in the 1990s that argued for a "eusociality continuum" that placed bees and humans on the same general scale of shared parenting behaviors.

But when she saw the scatterplot above, Lacey told Ars that she had to change her mind. "Science needs to be evolving if we're learning along the way, and OK, we learned more," she said with a laugh. Now she's convinced that evolutionary pressures have pushed social animals along two distinct pathways to monogyny or polygyny.

Two evolutionary trajectories

There are other clues beyond statistical correlations that suggest we're looking at two distinct strategies. Monogynous insects have a radically different life cycle than many polygynous animals. Ants and bees undergo profound physical transformations during their lifecycles, as they go from eggs to larvae to adults.

An ant's entire body plan will change based on the foods and chemicals it's exposed to as a larva, and the result might be a small forager ant or an enormous soldier ant. "It seems like it’s easier for natural selection to build in dramatic trip points to shut off reproductive access at one of those stages," Lacey explained. Indeed, it's during the larval stage that an ant or bee might be given food that triggers developmental changes so that she becomes fertile rather than defaulting to sterile. Polygynous animals don't seem to have these dramatic life stages. There's puberty, but that shift isn't as dramatic as what an ant experiences as it morphs from a larva to an adult.

Other differences are demographic, Lacey said. Many rodents and birds find their mates in a process called philopatry, where potential breeders hook up at a designated mating ground every year. But the way these mating grounds are organized varies a lot across species. Males and females may visit a special area every year, or roving males might return to a home base where females live. Evolutionary pressures, such as food availability or predators, can shape how species engage in philopatry; this in turn may be affecting whether the species becomes monogynous like naked mole rats or polygynous like house mice.

It's also possible that an evolutionary pressure to reduce competition between females led to the overall picture we're seeing, where a greater number of females leads to a smaller number of breeders.

Getting out of the continuum

Regardless of the evolutionary causes—and we'll need more research to find out what those are—it's clear that we're seeing two distinct evolutionary trajectories rather than a continuum of many. In their paper, the researchers conclude:

Under a scenario of qualitatively distinct evolutionary outcomes that are shaped by different selective pressures, we would predict a significant negative relationship between the proportion of breeders and the total number of females in a group (indicating that a predictable ratio of breeders to non-breeders is favoured by selection). By contrast, under a scenario of continuous variation in social structure, we would predict no relationship between the proportion of breeders and the total number of females in a group (i.e. species would occur anywhere in this parameter space).

Because we see such a predictable relationship between numbers of breeders and numbers of females in a given social group, it appears we do not live in a world of infinite choices when it comes to organizing our reproductive lives.

That said, co-author Rubenstein clarified that there is a continuum of sorts among polygynous species. "Within the polygynous/plural breeding species (i.e., those with more than one breeding female) there is essentially a range of values or a continuum," he told Ars via e-mail. "But there does not seem to be a continuum from monogyny/singular breeding to polygyny/plural breeding. In other words, those are two distinct strategies and not together on the same continuum." He also cautioned that more research needs to be done on social animals that live in smaller groups to see whether more robust patterns emerge as we have more data.

For now, however, this new paper offers a provocative way of looking at social patterns shared among dramatically different species. The more females there are in groups of social animals, the fewer individuals are actually reproducing. And in case you were wondering, this does not mean that humans who live together in megacities are going to start becoming all-female societies of sterile workers. "Cities are comparable to herds of wildebeests rather than eusocial animals," Lacey said. "[Urbanites] are forced together due to resource availability, but there's no internal structure to that herd."

Royal Society Open Science, 2016. DOI: 10.1098/rsos.160147