Why Forest-Dwelling Lionesses Seek Many Mates
(Inside Science) -- On a bright day in 2015, an Asiatic lioness hid her cubs in a thicket and went to meet two strangers. The strange males' roars echoed through the Indian forest, proclaiming their intent to drive out local males and claim new territory. Since they were new to the region, there was no way either of them could be the father of the lioness's cubs. If they found the cubs, they would kill them.
The lioness was still nursing, not ready to be impregnated again. But she knew all the moves -- how to nuzzle a male's shoulder and flick her tail in front of his nose as though she were in heat. When the invaders saw her performance, they followed eagerly.
The mother lioness led the two invaders about 2 to 3 kilometers away from her cubs, then gave one of the males what he expected: a day of flirting and occasional copulations. Male lions form tightknit coalitions, so the other male remained nearby. In the early morning when her lover was asleep, the lioness snuck away, carefully placing each paw to avoid dry leaves and snapping twigs. He awoke to find her gone.
"The guy lost it. He went berserk," said Stotra Chakrabarti, an animal behaviorist at the University of Minnesota in Minneapolis. "It was amusing, but it was also very frightening for us, because he's going to follow every noise. … And of course, we cannot be as silent as the cats."
It's common for lionesses to sneak away from trysts before a male is ready to part ways, said Chakrabarti. But normally, mating lions will spend two to five days together. Most of the action happens on days two and three, when the pair copulates an average of 50 to 70 times a day.
This lioness left after just one day. She returned to the cubs and then led them even farther away from the invading males. The following year, Chakrabarti saw a different mother lioness perform the exact same deception with two more invading males.
Chakrabarti's research is revealing the complex strategies Asiatic lionesses employ to keep their cubs alive. In many respects, lions in India face the same pressures as their better-studied counterparts in the Serengeti region of Africa. But while the Serengeti is a savanna habitat, Asiatic lions live in the forest, and that shapes everything from what they hunt to whom they associate with. It may also shape the way lionesses use their feminine wiles -- one of the only tools they have to protect their cubs from murderous males.
Asiatic lions are a subspecies of Panthera leo, genetically distinct from but part of the same species as their African kin. The Asiatic subspecies once roamed from Greece through the Middle East and well into India. Now, it survives only as a remnant population of about 600, confined to a 20,000-square-kilometer region in western India known as the Gir forests.
Chakrabarti and his colleagues have studied these lions for years, following them through the forest armed with only bamboo canes. ("If a lion charges at you, never show your back," said Chakrabarti. "You make a lot of noise; you stand your ground." He adds that the researchers try not to approach too closely, and nonprofessionals should keep their distance from lions.)
This month at a virtual meeting of the Ecological Society of America, Chakrabarti presented findings from a 2019 study in the journal Behavioral Ecology that revealed the hidden dramas of these lions' lives. The study is part of a long-term project led by Yadvendradev Jhala, a researcher at the Wildlife Institute of India.
The researchers combined detailed observations and tracking data from 70 adult lions living in the Gir forests, including 11 coalitions of males and nine prides of females. Coalitions ranged in size from one to four males, while prides consisted of three to eight females and their young.
The researchers found that males' territories overlapped the ranges of multiple female prides, and also frequently overlapped the ranges of other male coalitions. Each pride had one "primary" male coalition with which it shared most or all of its territory, and one to three "peripheral" coalitions with which it shared smaller slices of the forest.
Surrounded by all these males, the females were anything but coy. They engaged in an average of five to six mating events with two to three different males for every time they got pregnant. Each mating event consisted of several days paired off with a single male, copulating repeatedly.
About 64% of mating events were with members of a female's primary coalition, while 36% were with members of peripheral coalitions. The researchers only analyzed mating events during times of social stability. The two incidents when mother lionesses hid their cubs and seduced invading males weren't included in the statistical analysis, since they occurred during times when males were usurping each other and reshuffling territory boundaries.
Why would lionesses spread their charms so widely? It's possible they gain some genetic advantage by having different fathers for different cubs. Asiatic lions are highly inbred, and multiple fathers could help a lioness ensure diversity in her offspring, increasing the chances that at least some of them will have a winning combination of genes.
But researchers suspect another reason is that male lions are cub-killers.
Why males kill infants
Baby-killing is a fact of life for many of our mammalian relatives. One of the most common scenarios involves adult males targeting babies that were sired by their rivals. Since the mother no longer has an infant to nurse and care for, she can be impregnated again sooner, and the infanticidal male then has a chance of fathering her next baby.
This strategy may seem abhorrent to us, not to mention to the baby animals and their mothers. But natural processes aren't always nice. Any trait that helps an animal produce more surviving offspring will be favored by natural selection.
There is no scientific evidence that human men have instincts pushing them to kill infants so they can impregnate their mothers. But the consensus among biologists is that many male animals do have such instincts, especially among primates, rodents and big cats, said Sarah Hrdy, an anthropologist who is now retired from the University of California, Davis.
Lions are a classic example. Research from the Serengeti region in Africa has shown that when a resident coalition of males is ousted, the new males promptly kill or drive away any cubs they can find.
On the savanna, a coalition typically defends one or more prides from rivals for as long as it stays in power. The resident males protect the cubs from infanticide, but also prevent the females from mating with outsiders, according to Craig Packer, an ecologist at the University of Minnesota, who has conducted extensive research describing lion behavior in the Serengeti region and is now collaborating with Chakrabarti. When Packer and his colleagues conducted genetic testing on 78 lion cubs in the Serengeti region, they found that every single one had been fathered by a member of its resident coalition.
In contrast, Gir males spend much less time with females, and they aren't able to defend exclusive access to them. Females share their territories with multiple coalitions of males, any of which could pose a threat to their cubs.
Sex may be a way for females in the Gir forests to get all those males on their side. If a male has reason to think he may be the father of a cub, it is probably in his best interest to let it live.
In the Gir forests, the researchers found that none of the resident males from either primary or peripheral coalitions ever attacked cubs in their territories. When new males invaded the territory, they attacked every cub they encountered.
Chakrabarti said he is working on genetic testing that will reveal which males sired which cubs. Without that data, noted Packer, there's no way to know whether the males were sparing cubs because there was a real chance they might be the father, or whether some of them were "tricked" by the females.
Lionesses could be deliberately mating at times when they're not fertile. Moreover, there might be some way lionesses can prevent pregnancy even after they've mated. For example, they may be able to control whether they ovulate.
Interestingly, young Gir lionesses breeding for the first time rarely sought mates outside their primary coalition. Eighty-nine percent of the matings with peripheral males were by older, experienced females. It's not clear why the lionesses' strategies differed by age, said Chakrabarti. But it seems that as long as at least some lionesses have mated with members of a coalition, the entire pride is protected from that coalition. This may be because prides often raise their cubs communally, so males can't tell which cub belongs to which lioness.
Hrdy, who was not involved in the project but developed much of the evolutionary theory on infanticide and female counterstrategies, said she thought the study was well done and very welcome. It gave her pause, however, when the paper described taking multiple mates as a win-win for females. She views baby-killing as a form of sexual coercion, essentially canceling out a female's last mate choice so that she must mate with the killer or go childless. Females may be able to prevent some killings by mating with males in advance -- but that doesn't mean they are choosing freely.
"Nothing about this is a win-win," said Hrdy. "Females are using mating with multiple males as the only card they can play in a game that otherwise is heavily rigged toward males."
The power of habitat
Lions are far from the only species in which females are thought to use sex to reduce the risk of infanticide. A study by Maria van Noordwijk and Carel van Schaik found that males routinely kill infants in 40 carnivore species and 47 primate species -- the majority of carnivores and primates for which data were available. Females are much more likely to mate with multiple males in species where males pose a threat to infants.
Asiatic lions offer a rare opportunity to see how animals' environments affect such strategies. While lions everywhere follow the same basic template for behavior and lifestyle, there are differences between the Gir and African savanna populations, and those differences probably aren't due to any differences in genetics, according to Chakrabarti and Packer.
Researchers suspect the key to the differences lies in what lions eat. On the savanna, lions hunt large animals like wildebeest and zebra, which can feed five or six lions at a time. If males are around when females make a kill, they will insist on eating first, but everyone still gets a share.
"There's enough food there to feed your husband as well as your sister," said Packer.
In the Gir forests, on the other hand, prey animals are smaller. If males show up at a lioness's kill, chances are there will be nothing left for her. Sensibly, Gir lionesses seem to avoid males most of the time, perhaps aided by concealing forest foliage, said Chakrabarti. In previous work, Jhala and his colleagues found that lionesses often hunt when males are resting.
Since males spend so much time apart from females, they likely have trouble keeping other males away, said Packer. Surrounding coalitions can easily sneak in and get access to lionesses and their cubs. Thus, the researchers suspect the forest encourages a social system in which females have ample opportunity to mate with different coalitions of males -- and, given the risk of infanticide, ample reason to do so.
"I think that's what's really interesting about this study, that you make the full link between 'where do they live' to 'how do they behave,'" said Dieter Lukas, an evolutionary biologist at the Max Planck Institute for Evolutionary Anthropology in Germany, who was not involved in the study. "We can try to understand what it is about the environment that influences something such as the mating behavior."
Mysteries remain, including the precise motivations of the lioness who lured invading males away from her cubs in 2015. Chakrabarti is skeptical that the male she seduced would believe the cubs were his, given that they were already around 4 months old. It's possible the lioness was just removing the immediate threat, like a bird luring a predator from its nest by pretending to have a broken wing.
But the primary reason males kill cubs is so they can breed with their mothers sooner, noted Lukas. Perhaps the lioness was signaling to the male that she was already prepared to have his cubs, lessening his motivation to kill her current litter.
It took a while for the two cubs to emerge from their hiding place when their mother returned, said Chakrabarti. The lioness strode up and down the thicket, humming gently. Her pride-mate appeared first, a female about 3 or 4 years old. Finally, her young son and daughter toddled out, to be greeted with head rubs and licks.
The female cub died soon after, passing away from some unknown health problem. The male cub grew up strong. When he was 2 and a half, he struck out on his own: a living embodiment of his mother's success.