Why Male Mammals Choose Monogamy

A male dik-dik antelope closely follows the female as she searches for food in her territory, guarding her against other males. [Courtesy of Peter Brotherton]

In perhaps the most comprehensive and definitive effort to date, scientists have explained the processes that drove male mammals to adopt social monogamy as a breeding strategy.

Because male mammals have a much higher potential to produce offspring in a single breeding season than do their female counterparts (who must endure long gestation periods), it would seem that mating with one female per cycle would be limiting. Yet a percentage of mammalian males do this — and researchers have debated why, seeking to identify selective advantages social monogamy offers, for decades.

"People have been interested in the evolution of monogamy in mammals for over thirty years," said the study's senior author, Tim Clutton-Brock of the University of Cambridge, UK, whose research appears in the 2 August issue of Science.


Press teleconference with the authors 29 July. [AAAS/SciPak]

"In the last ten years alone," continued first author Dieter Lukas, also of the University of Cambridge, "there have been perhaps 15 comparative studies, reviews, or books that have investigated alternative explanations for the evolution of monogamy in mammals." None provided conclusive answers, however.

More recently, the evolution of social monogamy in mammals has been explained by two prominent hypotheses, one of which focuses on paternal care, suggesting that natural selection favored pair-forming because care from two parents increases the fitness of offspring. The second hypothesis suggests that males form pairs to guard their mates.

Now, to better understand which hypothesis is more accurate, Lukas and Clutton-Brock have used data on more than 2,500 mammalian species to test the two, offering strong support for the second.

The authors were able to leap forward in their research compared to previous efforts with the help of gene-based phylogenies, the tree-like genetic maps that researchers use to infer relationships between species and understand in what common ancestor of a species a shift in breeding strategy occurred.

"Fifteen years ago," said Clutton-Brock, "this approach would have been impossible."

He explained that while several previous studies have used gene-based phylogenies to explore when in mammalian evolution males turned to social monogamy, their scope was not large enough — either in sample size or diversity of taxonomic group.

Relying on a very large sample, as well as a clear definition of social monogamy, Lukas and Clutton-Brock were able to weigh in more definitively. They started by compiling data on the observed distribution of social monogamy across current mammalian species.

"It took about two years, on and off, to collect the data on the social systems," said Dieter Lukas. "We searched for information for every known mammal (there are 5,400 species), consulting multiple sources, and we discussed our classification with researchers who are conducting field studies."

In total, more than 2,500 species of mammal are represented in their analysis.

Using detailed life history data, the researchers classified each species as either solitary, socially monogamous, or group-living, taking special care to include relevant species previously left out of the socially monogamous group. They then "forced" transitions to social monogamy from group-living females and solitary females, respectively, using statistical models to determine which transitions performed better.

In this context, "forcing" transitions to social monogamy from an alternative breeding system means the researchers only considered processes in which changes to social monogamy occurred from that breeding system. This approach provides the likelihood of such a process to explain the distribution of social monogamy observed today.

The researchers identified 61 transitions necessary to explain the existence of social monogamy among mammals. Notably, all but one of these arose from ancestral species with solitary females — those who established home ranges in order to avoid competition with other females.


In groups of meerkats, the majority of individuals are the offspring of a single, life-long mated pair. [Courtesy of Dieter Lukas]
 
Further analyses confirmed that social monogamy is almost wholly derived from ancestors where females are solitary, not from mammals engaged in group living.

This finding informs the setting in which social monogamy evolved for male mammals; it's likely that males, unable to roam far and wide to defend access to more than one female, formed pairs. This helped them overcome the disadvantages related to the wide spacing of potential mates. The results support the second hypothesis of social monogamy as a mate-guarding strategy.

Unlike in previous studies, which found no significant difference in population density between socially monogamous females and those where females live solitarily, these authors showed that the former type of female occurs at lower densities today, and with less overlap with neighbors, than females in solitary species. This is likely because socially monogamous females require more energy-rich food, which is less plentiful, and perhaps are less tolerant of other females, too.

This insight also informs the setting in which social monogamy evolved, explaining the spatial distribution of females, which males had no choice but to follow. Guarding one mate was their best bet.

The evolution of paternal care, meanwhile, though it characterizes most socially monogamous species today, was a secondary adaption, the authors suggest.

A second study on the evolution of monogamy appeared in the journal PNAS this week and though it also suggests that paternal care is a consequence, not a cause, of social monogamy, it offers a somewhat different conclusion with respect to the ultimate driver of this breeding strategy in mammals. Looking at life-history data across 230 primate species and using similar methods (i.e., gene-based phylogenies), Christopher Opie of University College London and colleagues concluded that the threat of infants being killed by unrelated males is the key driver of social monogamy, at least in primates. Lukas and Clutton-Brock, meanwhile, found no association between social monogamy and infanticide, even after limiting their study to primates.

One possible explanation for the papers’ differing conclusions is the classification scheme used by each group to define just what a socially monogamous mammal is. The other possible explanation is sample size; that of Opie and colleagues involved approximately ten times fewer transitions to social monogamy for researchers to study, and from which to draw conclusions. In days ahead, the authors of the two papers may come together to investigate these differences.

Neither of the Science authors found their results surprising. "What did surprise me," said Lukas, "was what I observed during data collection — the number of different species for which there are observations on natural behavior. The dedication and hours that it must have taken researchers during the past 100 or more years to go out and observe animals is impressive. And it is important that these field-based studies continue," he explained. "Except for key charismatic species such as primates, detailed information on the biology of the vast majority of mammals is only now starting to become available."

Having used more than 2,500 species of mammals from all orders, this study is very comprehensive. "One next step would be to test whether similar ecological pressures were involved in the evolution of social monogamy in other taxonomic groups," explained Lukas.

It should be noted that this study does not provide insights into when, and under which circumstances, monogamy evolved in humans. "It could potentially have evolved during a stage in which ecological factors led to females becoming separated and solitary," Lukas explained, "but it is also possible that monogamy is a very recent, cultural arrangement of marriage within groups. Anthropologists have started to apply phylogenetic approaches to infer when during the history of human cultures changes in the mating system are likely to have occurred, but, as yet, there is no clear answer."

Read the abstract, “The Evolution of Social Monogamy in Mammals," by D. Lukas and colleagues.