Before a pair of zebra finches can settle down to start a family, they have to find a place to live. Whether that’s up in a tree or in a constructed nest box, the responsibility for finding a good nest site typically falls to the male—though the female’s opinion can make or break a decision. “The male will kind of go from one nest site to the next, and they’ll check it out together,” explains evolutionary biologist Kerianne Wilson, who spent hundreds of hours during the 2010s observing the behavior of zebra finches in aviaries as part of her PhD at the University of California, Irvine. “If the female doesn’t like it, she’ll leave,” in which case the male will usually “have to coax her into house-hunting again.”
Disagreements about potential nest sites can crop up for various reasons, Wilson says. Aggressive neighbors are a particular irritation for communal songbirds such as zebra finches (Taeniopygia guttata), which typically live in colonies of several dozen members. But individual birds differ in their assessments of the pros and cons of a particular nest site, and it’s here that problems can arise for socially monogamous zebra finch couples, which live together and share parenting responsibilities as they raise multiple cohorts of young. Some pairs simply seem to be incompatible in the house-hunting department, Wilson says, leading to protracted searches. These birds risk missing out on a good, or at least a passable, nest site. If the male and the female “really can’t get on the same page,” they may in rare cases end up trying to raise their young across two different nests, Wilson says. More often, though, incompatibility in nest preference foreshadows a more decisive outcome: divorce.
In recent experiments with flocks kept in aviaries in California, Wilson and colleagues studied the behavior of zebra finch pairs—identifiable by bonding behaviors such as snuggling up to each other, grooming, and joint house-hunting—that were exposed to unfamiliar individuals during the breeding season. Finches were more likely to split up with their current partner and get together with a new one if the bonded pair had visited a higher number of nest sites, the team found.
If a mate ends up being a good partner, you’ll want to mate with them again, conceivably, because you had great fitness.—Kerianne Wilson, University of California, Riverside
The group’s study, which was published online late last year, is one of just a handful of projects that have experimentally investigated the reasons that pairs of monogamous animals split up. Indeed, divorce—or mate switching, to use a less anthropocentric term—received relatively little research attention until a few decades ago, despite being described in a number of species throughout the 20th century. One reason for that could be that the full complexity of animal mating systems has only become clear thanks to genetic studies, notes Antica Culina, a senior scientist at the Ru?er Bošković Institute in Croatia and an honorary fellow at the Netherlands Institute of Ecology. Researchers have been forced to update traditional descriptions of monogamy—once defined as “a system where males and females form some kind of bonds and then they’re relatively exclusive,” says Culina, whose PhD at the University of Oxford focused on divorce in birds—in light of genetic data showing that many supposedly monogamous animals actually produce young with a much greater number of partners than researchers have observed them with.
This recalibration has led to new distinctions between genetic monogamy (reproductive fidelity to a single partner) and social monogamy (shared parenting and other behaviors for a sustained period of time). It’s also renewed interest in the demographic and environmental factors that make or break animal couples, particularly among species of birds, which have a far higher rate of social monogamy—around 90 percent of species—than any other group of vertebrates. A small number of long-term observational studies are trying to uncover those factors, understand the costs and benefits for the individual animals involved, and even measure how divorce rates change over time—potentially affecting the size and survival of populations. From an “evolutionary standpoint,” says Wilson, now a postdoc at the University of California, Riverside, it all “helps us understand . . . what makes individuals more successful or less successful based on the pairing they have.”
VARIETIES OF MONOGAMY
Animals such as birds that live and raise young in pairs were once considered to be monogamous in all senses of the word—they exclusively live and mate with one other individual. However, genetic studies over the last few decades have revealed that many of these species are not exclusive, mating with individuals outside their pair. This revelation has led researchers to distinguish between genetic and social monogamy.
© michelle kondrich
SOCIAL MONOGAMY: When individuals form social bonds and perform behaviors such as parenting in pairs, but don’t necessarily mate exclusively
EXTRA-PAIR PATERNITY: When a male fathers offspring outside of his social pair
GENETIC MONOGAMY: If a bonded pair only has offspring together, i.e., there is no extra-pair paternity
Why are you leaving?
In 1987, two researchers in Ontario produced a detailed review of divorce among gulls (family Laridae). In it, the scientists considered multiple published accounts of apparently monogamous birds leaving their partners, both within breeding seasons—often after an initial clutch of eggs had been destroyed or eaten by predators—and between breeding seasons, during which time members of a partnership might migrate to overwinter in different parts of the world. The rates of divorce varied, the authors noted, with some species such as silver gulls (Chroicocephalus novaehollandiae) seeming to switch mates relatively rarely, while more than a third of pairs in other species, such as Caspian terns (Hydroprogne caspia), divorced between one breeding season and the next.
Longer-lived species tend to have lower divorce rates, perhaps because they benefit more from built-up familiarity over multiple rounds of producing and rearing offspring.
In the decades since then, says Culina, scientists have come to appreciate divorce as an almost universal trait of monogamous species. A famous table published in “Mate Fidelity and Divorce in Monogamous Birds,” the concluding chapter of a 1996 book edited by ornithologist Jeffrey Black entitled Partnerships in Birds: The Study of Monogamy, revealed a huge range in divorce rates. Among the loyal geese and swans, about 5 percent of pairs split up between seasons, while among passerines such as Eurasian blue tits (Cyanistes caeruleus), nearly 50 percent of pairs split per year on average. Across socially monogamous animals, in fact, “you have from zero to a hundred percent divorce rates, but most species are somewhere in between,” Culina says. “It really depends on the life history of the species.”
Several factors correlate with average divorce rates in animal species. One is lifespan: longer-lived species tend to have lower divorce rates, perhaps because they benefit more from built-up familiarity over multiple rounds of producing and rearing offspring, Culina says. Another is mortality: species with high mortality rates divorce more, perhaps because there are more widows and widowers to potentially woo paired individuals away from their partners. Some research suggests that species with higher female-to-male sex ratios also tend to have higher rates of breakups. These species-level factors can go only so far in explaining why an individual stays or leaves, however. Studies like Wilson’s, which follow individual pairs, are needed to offer new insights into the drivers of divorce as a behavior.
Sometimes, of course, divorce might be a matter of circumstance more than choice. In the case of birds that make long migrations during part of the year, members of a pair might arrive at breeding sites at different times, or not at all, notes Chris Redfern, an emeritus professor at Newcastle University in the UK who has studied the annual journeys of arctic terns (Sterna paradisaea) from North Sea islands off the coast of the United Kingdom down to East Antarctica and back. In these species, it’s common for the bird that arrives first, after flying tens of thousands of kilometers across hemispheres, to find another mate rather than wait too long for their partner and miss the chance to reproduce, Redfern says.
Related explanations have been invoked to explain divorce in some mammalian species. In socially monogamous primates such as Azara’s owl monkeys (Aotus azarai), for example, divorce may be forced by the arrival of new aggressive individuals to a group, while in alpine marmots (Marmota marmota), research suggests that partner switching likely results from one member of the breeding pair dying or fleeing from conflict with other marmots. In these cases, divorce appears to be driven more by external factors than by individual decision making, and there may be costs to divorcees in terms of the time needed to establish a new partnership or lower reproductive success.
Yet a large volume of theoretical and experimental work on divorce holds that leaving one partner for another, even when the original partner is available and ready, could also be an evolutionarily beneficial strategy that allows individuals to seek a better mate. In a recent lab study of lined seahorses (Hippocampus erectus)—monogamous fish that show synchronized swimming and other pair-bonding behaviors when coupled up—researchers found that females were more likely to switch partners if the male, which carries the offspring, was injured or sick. In these cases, the female would often start courting new males even as her current partner carried her eggs. This idea of trading up has been proposed to explain many cases of divorce in birds, too—as a way to ditch mates that only produced a few viable offspring, for example, or that didn’t pull their weight in parental care. “If a mate ends up being a good partner, you’ll want to mate with them again, conceivably, because you had great fitness,” says Wilson. “But if you had poor fitness then you’re basically behind,” and so switching away from the low-quality partner makes sense. This explanation has been cited a number of times in studies from the last few decades—including in a recent study of seabirds that found that black-legged kittiwakes (Rissa tridactyla), which brood one to three eggs a season, were more likely to divorce if they had had a breeding failure, such as eggs not hatching or young chicks dying.
Not all tests of this hypothesis have been straightforward, however. A recent observational study of snowy plovers (Charadrius nivosus) in Mexico found that pairs were more likely to split up after a successful nesting, with females in particular often deserting their broods to pair up with different males. A follow-up study by the same researchers found that this behavior was prevalent across various plover species around the world, and that divorcees tended to have more offspring overall than birds that stuck with their original partner. The work “provides a counterpoint to theoretical expectations that divorce is triggered by low reproductive success, and supports adaptive explanations of divorce as a strategy to improve individual reproductive success,” the authors note in their paper.
Studies such as these speak to the challenges of drawing general conclusions across species or even populations of the same species. Culina points out that “we have good evidence that divorce can lead to an increase in breeding success and so fitness benefits, but we also have evidence that in some situations it will decrease fitness. And in some situations, it will just be neutral.”
There may often be confounding factors, too, says Stéphanie Jenouvrier, a seabird ecologist at the Woods Hole Oceanographic Institution. Some species, such as the snow petrels (Pagodroma nivea) that she studies, combine monogamy with other behaviors, such as fidelity to particular nest sites. Petrels compete for nest space in crevices in cliffs along Antarctic coastlines, areas that can vary in their susceptibility to freezing over or being flooded by melted snow. Both conditions damage the nest, she explains, and in these cases, “some birds may divorce . . . not necessarily to leave their partner, but to leave the nest.”
You have from zero to a hundred percent divorce rates, but most species are somewhere in between.—Antica Culina, Ruder Boskovic Institute
Such complications make tests of divorce as an adaptive behavior a significant challenge, says Wilson. Indeed, biologists have argued that for divorce to be a truly adaptive behavior, subject to natural selection, it has to be a heritable trait that varies in the population, but that’s been difficult to demonstrate. One recent study that attempted to address this issue used 39 years’ worth of breeding records for song sparrows (Melospiza melodia) on an island off the west coast of Canada. Analyzing a total of 166 breakups among 566 different pairs, researchers found that some females were indeed more likely to split from their partners, but the team saw no such pattern in males. Statistical modeling also suggested that tendency toward divorce might be somewhat heritable across generations, although probably not enough to allow rapid evolutionary changes in the population, the researchers concluded in their paper.
Even these studies are difficult to interpret, says Culina, as scientists often don’t know for sure which individual initiated divorce or why. Rather than being inherently more likely to walk out, “if some individuals show consistently high divorce rates, it might also be that they are just low-quality individuals that have been [repeatedly] divorced by others.” In other words, rather than “a gene for divorce . . . it might rather just be a gene for other traits that make you less attractive, and that’s why you’re always being left by your partner.”
Long-term data on divorce patterns and on lifetime survival and reproductive success of individual animals are needed to draw meaningful conclusions about the costs and benefits of splitting up, experts agree. Studies now underway could provide such data while yielding clues about how divorce rates could change through time—and perhaps influence a population’s stability.
A SAMPLING OF MONOGAMOUS VERTEBRATES
Not many animals maintain monogamous relationships, and almost all studied examples of monogamy are in birds. Below are some examples of species that do form socially and/or genetically monogamous pairs.
© michelle kondrich
Although little is known about mating systems in sharks and other cartilaginous fishes, there is evidence that some species such as tiger sharks (Galeocerdo cuvier) could be genetically monogamous.
Most fish species are promiscuous, but some, such as seahorses (genus Hippocampus), are genetically and socially monogamous, with pairs mating and sharing parental care for most or all of their lifetimes.
Monogamy was thought to be absent from the amphibian clade, but in 2010 researchers published evidence of social and genetic monogamy in a Peruvian poison dart frog (Ranitomeya imitator).
Few reptiles are monogamous, but one exception is the Australian shingleback lizard (Tiliqua rugosa), which forms social relationships for 20 years or more—although around one-fifth of individuals have extra-pair relationships too.
Social monogamy is found in around 80–90 percent of bird species, although extra-pair mating is common. Albatrosses (family Diomedeidae) famously form strong social bonds that can last for decades.
Fewer than 1 in 10 mammalian species practice some sort of monogamy. The socially monogamous prairie vole (Microtus ochrogaster), which forms close bonds and even shows anxiety-like behaviors when separated from a partner, has become a well-studied model organism in research on monogamy, though they often mate with individuals other than their partner.
Every September in the Falkland Islands off the south coast of Argentina, some 500,000 pairs of black-browed albatrosses (Thalassarche melanophris) settle down to raise the next generation. These huge seabirds are famous for their long-term relationships: many form lifelong partnerships over their multi-decade lifespan. Hundreds of breeding pairs on one of the islands have been tagged and monitored at the site since 2003, with GPS data added for some individuals from 2008. When marine ecologist Francesco Ventura had the chance to study these pairings a couple years ago as part of his PhD at the University of Lisbon, he saw an opportunity to ask an unusual question: Do environmental changes influence a bird’s decision-making about its partner?
Sifting through the breeding records, he and his colleagues found that, on average, only around 4 percent of pairs divorced per year over the 15-year study period, and that was typically after a breeding failure, consistent with the idea that birds such as albatrosses split up to seek higher-quality mates. However, combining the data with measures of environmental conditions, Ventura and colleagues found that the rate of mate switching showed a clear link with ocean temperature variability, even when controlling for breeding failures and the number of birds whose mates had failed to return to the breeding site. Specifically, in years where there had been anomalously high sea-surface temperatures, something that’s become more common as a result of climate change and is associated with reduced food availability for many seabird species, there were also spikes in the number of divorces.
Long-term data are needed to draw meaningful conclusions about the costs and benefits of splitting up.
Ventura says he thinks that the environment is essentially “misinforming” birds’ decisions about whether to stay or leave. Specifically, bird parents struggling through a difficult breeding season due to lack of food and physiological stress “might misinterpret the poor performance by the mate as poor parental abilities.” Given that the challenges are instead the result of a poor environment, there’s no obvious benefit to switching mates, and in fact it could be deleterious in the long run, as divorcees must incur the costs of establishing bonds with a new partner. While the albatross population Ventura studies is large and shows no sign of shrinking, these kinds of changes in divorce patterns could have a larger effect in smaller populations, particularly if there’s a low availability of alternative mates. “If you think about it in that context,” Ventura says, “that might definitely introduce much more disturbance in the breeding processes,” adding that this should be the subject of future research.
Only a few studies have tried to parse the influence of environmental factors on divorce rates in other species, but already numerous hypotheses have emerged. For example, researchers such as Redfern have speculated that there may be additional effects of climate change on birds such as arctic terns that spend part of the year on long migratory journeys to find food. He and a colleague have observed changes in terns’ movement patterns in the Antarctic in recent years, possibly relating to changes in sea-ice coverage in the region. If food becomes harder to find in the Antarctic, it could make terns’ arrival times back at their breeding grounds in the North Sea more variable, which may in turn increase divorce rates there too.
Jenouvrier, meanwhile, is analyzing data on the effects of climate on snow petrel behavior. Because ice formation and snowmelt can destroy these birds’ nests, she notes, she and her colleagues are hypothesizing that they’ll see a relationship between Antarctic conditions and the number of petrel divorces. Zebra finches may be affected by a changing environment too: Wilson notes that shifts in the birds’ geographical range—e.g., poleward as the climate warms—could potentially influence interactions between individual colonies. Based on her findings, if there’s more intergroup mixing, “we could conceivably see higher divorce rates,” she speculates, adding that such a change “could take an unforeseen toll on the population.”
For now, the true costs and benefits of changing divorce rates are murky. Evolutionary theory doesn’t provide much help here, Culina notes, as different models support different predictions. One idea is that “if the environment changes . . . it’s better to have more genetically diverse offspring because then you have a higher chance that one of them or some of them survive the new environment,” she explains. “But there’s also this idea that if you change your partner and the environment changes too, that you lose, because you’ve lost your familiar partner with whom you might be able to socially cope better in the new environment.”
Editor’s note (June 1): Evolutionary biologist Kerianne Wilson informed us that the main image originally accompanying this story depicted two male zebra finches. The page has been updated with a photo of a male and a female to better reflect the research described in the article.