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IMAGINE spending four months upside down, half starved, babysitting a brood of tiny eggs under a leaf. Parenting is tough for daddy longlegs living in the Brazilian Atlantic forest, but their efforts aren鈥檛 in vain. Having a parent to watch over the eggs makes a huge difference to their survival; .

Although we humans no longer need to protect our progeny from hungry predators, we are accustomed to thinking that parenting is crucial if offspring are to survive and thrive. Yet, among the myriad organisms on our planet, this is rare. What鈥檚 more, in those species that do care for their young there is a strong bias towards females doing all the work. That makes the daddy longlegs a real oddity 鈥� it is among the few examples where males alone raise the young.

When it comes to parenting, why do some males buck the trend and take the lion鈥檚 share? This question has puzzled scientists from Charles Darwin onwards. They have come up with some ingenious theories, but as we have learned more about nature鈥檚 devoted dads, several have fallen by the wayside. We do know that male parental care has evolved independently many times, in a diverse array of animals. Interestingly, exclusive care by dads is clustered in some branches of life鈥檚 evolutionary tree, including certain fish and frogs. Each species may have its own story, but the example of the daddy longlegs highlights a surprising common thread. While babysitting, daddy longlegs fathers can receive the amorous attentions 鈥� and eggs 鈥� of up to 20 females and, . In other words, childcare isn鈥檛 just a chore for doting dads: it has its perks.

鈥淐hildcare isn鈥檛 just a chore for nature鈥檚 doting dads: it has its perks鈥�

The idea that most parenting falls to mothers was self-evident to Darwin. He was perplexed by species in which males cared for the kids. In The Descent of Man, and Selection in Relation to Sex (1871) he writes that the male emu, 鈥渘ot only performs the whole duty of incubation, but has to defend the young from their mother鈥�. He provides the amusing, if dated, anthropomorphic comment that in emus, 鈥渨e have a complete reversal not only of the parental and incubating instincts, but of the usual moral qualities of the two sexes; the females being savage, quarrelsome, and noisy, the males gentle and good鈥�. Darwin also noted that among species where males care for offspring, females often actively seek out mates, reversing the typical pattern of males fighting for females. Building on this observation, he proposed two explanations for such behaviour. Males may have 鈥渓ost their ardour, so that they no longer search eagerly for their females鈥�, putting their efforts into raising their offspring instead. Alternatively, 鈥渇emales have become much more numerous than the males鈥�[so that] it is not improbable that the females would have been led to court the males, instead of being courted by them鈥�.

Darwin鈥檚 line of thinking, invoking sexual selection rather than natural selection, carried through right up until the 1980s. One man who went against the grain, however, was evolutionary biologist Robert Trivers. In 1972, while at Harvard University, he proposed that parenting practices are underpinned by a basic physiological difference in most species 鈥� unequal gamete size. The energetic costs of producing large eggs versus tiny sperm means that from the outset females have invested more in offspring, and caring for young helps them protect that investment.

Trivers鈥檚 idea was hugely influential. However, critics pointed out that such a strategy does not make sense from an evolutionary perspective. Future and current investment should not be based on past investment, but rather on the promise of future pay-offs, says Charlotta Kvarnemo at the University of Gothenburg, Sweden. The British and French governments made this mistake when they continued investing in the supersonic aircraft Concorde even when they knew it would not make a profit. Indeed, the idea that parental care can be explained by past investment has . Modern biologists realise that when it comes to parental investment, it is the future that matters, not the past.

Left holding the baby

But Trivers had a separate explanation for doting fathers, which came from the observation that single fatherhood is common in species where egg fertilisation occurs outside the body. His 鈥渃ruel bind鈥� hypothesis is based on the idea that whichever sex deposits its gametes last gets stuck looking after the young. In fish that reproduce using external fertilisation, that falls to dads, because females extrude the eggs and then males fertilise them. Neat idea, but over time the hypothesis fell out of favour. The problem with the original idea, says Hanna Kokko, a mathematical ecologist at the Australian National University in Canberra, is that in some species with paternal care, , too small a time difference to matter.

So what is going on? Newer mathematical models offer some alternative explanations. One reason a male fish might hang around after releasing sperm is to prevent rivals from getting close and fertilising the eggs. Models created by Kokko鈥檚 student Andrew Kahn suggest that this so-called paternity guarding could have led to the evolution of more extensive fathering (). His haiku encapsulates the idea: 鈥淏lock that guy鈥檚 sperm man! Wait, where did that female go? You鈥檙e stuck with the kids.鈥� It doesn鈥檛 even matter if some of the young are not his. Kvarnemo has calculated that, provided males mate with several females and offspring have a high survival rate, paternity doesn鈥檛 need to be high for male care to evolve. What鈥檚 important, says Kvarnemo, is not the percentage of eggs a male has fertilised, but the total number that are his.

Another factor influencing parental care is cost to the carer, according to Kokko鈥檚 models. In many birds, parents stuff food into the mouths of each offspring separately, a job that in 90 per cent of species is shared by two parents, sometimes with helpers. Single parents are rare, and .

In one group of fish it is a different story. Among teleosts, the group of bony fish that includes most commonly eaten species, although parental care is rare, where it does exist, males do it by themselves nine times as often as females. Such care usually involves nest-building and defence, with fin-fanning movements used for security patrols also aerating the eggs. Such multitasking, together with the fact that they do not have to feed the young, means energy expenditure is relatively low. What鈥檚 more, it is not much more costly to care for 100 eggs as for 50.

Fishy fatherhood is not only cheap, it is also rewarding. Fertile females still come a-calling at a male鈥檚 nest. 鈥淭here鈥檚 no sexual jealousy in fish,鈥� says Kokko. And when there is no strict trade-off between mate attraction and care, male care is more likely, she adds. Indeed, females often prefer to mate with a male that is already looking after eggs, probably viewing this as a sign of his caring credentials. Besides, her eggs may be safer if deposited among oodles of others because when a tethered dad gets hungry, he often eats some of his brood.

鈥淲hen a babysitting dad gets hungry, he often eats some of his brood鈥�

Cannibalism of one鈥檚 own offspring is anathema to us, but Hope Klug at the University of Tennessee, Chattanooga, thinks it could have helped in the evolution of parental care. 鈥淚t gives parents, and particularly males, a way of adjusting how long they care for the clutch. It鈥檚 also a way of recouping some energy,鈥� she says.

This idea seems to be supported by some of nature鈥檚 most extreme dads 鈥� seahorses and pipefish 鈥� where paternal care even extends to male pregnancy. In the broad-nosed pipefish, for example, after a long courtship, the female transfers eggs into the male brood pouch, where they are fertilised and begin to develop. Using radioactively labelled amino acids, Kvarnemo showed that blood vessels in the pouch not only transfer nutrients from the father to the growing embryos, but also in the other direction. .

The Lusitanian toadfish is another example. Males of this species chorus like frogs to attract females to spawn with, then spend three to four weeks caring for the eggs, which are attached to the ceilings of their nests. Aside from the normal duties of aerating the eggs and chasing away predators, if the nest becomes exposed during low tide they dig underneath it and splash water on the eggs to prevent dehydration. It is hard work, says Clara Amorim at Lisbon University Institute, Portugal, and they are devoted fathers, but she has found that they do occasionally eat their eggs.

Fish fatherhood appears to have evolved because dads have much to gain and little to lose from caring. When it comes to other animals, the benefits are less well known, but some other factors influencing parental care have been identified. In recent decades it has been fashionable to look for ecological explanations based on things such as environmental conditions and resource availability. Among species of the poison frog genus Dendrobates, for example, parental care correlates with the size of the pool in which tadpoles are raised. In large pools, dads tend to care for young alone, carrying them around in mucus backpacks, whereas in tiny pools both parents get involved. When Jason Brown at the City College of New York looked at the genetic relationships between various Dendrobates species, he found that .

Asside from these colourful frogs, however, field tests frequently thwart notions that parenting styles reflect ecological factors. There are simply too many exceptions to the rules. In shorebirds, for example, species with reversed and conventional parental roles are found living side by side in range of habitats as diverse as Arctic tundra and tropical swamps.

Outnumbered

Still, the parenting practices of shorebirds suggest another explanation for devoted fathers 鈥� and one that turns Darwin鈥檚 thinking on its head. Far from male-based care occurring when females are more common, Tam谩s Sz茅kely at the University of Bath, UK, and colleagues found it had . In birds such as jacanas, females are polygamous and compete with one another for mates, while males, once mated, care for the offspring rather than take their chances on finding another mate. In other species, including the Kentish plover, parenting behaviour even varies from one population to another, with males taking more responsibility the more they outnumber females.

鈥淭he parenting practices of shorebirds turn Darwin鈥檚 thinking on its head鈥�

Does a biased sex ratio also help explain the parenting style of fish, frogs and invertebrates? It鈥檚 likely, but we don鈥檛 know yet, says Sz茅kely, because for many species there is not enough information on either mating systems or sex ratios to test the idea. Even if it does apply more widely, it is likely to be just one explanation among many. For Sz茅kely, answers are most likely to come by thinking big 鈥� about what males and females are doing across the whole population. But he acknowledges that this is easier said than done while .

We are still far from converging on a unifying theory of fathering 鈥� if one even exists. 鈥淧ersonally I don鈥檛 believe that there is one correct hypothesis,鈥� says Kokko. But if devoted dads remain a bit of a mystery, we have learned at least one thing since Darwin鈥檚 day 鈥� being a good father has its benefits.

See more in our gallery: 鈥�Six of nature鈥檚 most devoted dads鈥�

This article appeared in print under the headline 鈥淭he father enigma鈥�