42 | NewScientist | 14 June 2014

14 June 2014 | NewScientist | 43

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’t in vain. Having a parent to watch over the eggs makes a huge difference to their survival; without one, a third of clutches are eaten.

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’s 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 – 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’s 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’s 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’s 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 – and eggs – of up to 20 females and, hidden away from danger, their chance of survival is high. In other words, childcare isn’t just a chore for doting dads: it has its perks.

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, “not only performs the whole duty of incubation, but has to defend the young from their mother”. He provides the amusing, if dated, anthropomorphic comment that in emus, “we have a complete reversal not only of the parental and incubating instincts, but of the usual moral qualities of the two sexes;

THE FATHER ENIGMA

Nature contains some truly devoted dads but why should fathers care at all, wonders

Lesley Evans Ogden

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the females being savage, quarrelsome, and noisy, the males gentle and good”. 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 “lost their ardour, so that they no longer search eagerly for their females”, putting their efforts into raising their offspring instead. Alternatively, “females have become much more numerous than the males…[so that] it is not improbable that the females would have been led to court the males, instead of being courted by them”.

Darwin’s 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 – 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.

“ Childcare isn’t just a chore for nature’s doting dads: it has its perks”

44 | NewScientist | 14 June 2014

Trivers’s 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 come to be known as the “Concorde fallacy”. Modern biologists realise that when it comes to parental investment, it is the future that matters, not the past.

Left holding the babyBut 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 “cruel bind” 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, males release sperm just milliseconds after females release eggs, 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’s student Andrew Kahn suggest that this so-called paternity guarding

could have led to the evolution of more extensive fathering (Evolution, vol 67, p 2207). His haiku encapsulates the idea: “Block that guy’s sperm man! Wait, where did that female go? You’re stuck with the kids.” It doesn’t 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’t need to be high for male care to evolve. What’s 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’s 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 exclusive male care occurs in only about 1 per cent of birds.

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’s 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’s nest. “There’s no sexual jealousy in fish,” 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.

Cannibalism of one’s 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. “It gives parents, and

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“Humans are not very typical mammals, but they are quite typical birds,” quips Hanna Kokko at the Australian National University in Canberra. In about 90 per cent of mammals, the male’s role in reproduction stops at fertilisation – he couldn’t care less what happens after that. “Birds, in contrast, have pair bonds, extra-pair copulations (as we call them politely) and divorce. They have all kinds of complicated social relationships, not so unlike humans,” says Kokko.

But why do human fathers care for their offspring? Anthropologist Lee Gettler at the University of Notre Dame in Indiana points out that the contribution fathers make runs the gamut from deadbeat to devotee. “Paternal investment is highly variable within and across cultures,” he says. This has led him to describe paternal care as “facultative”. “Mothers are not routinely explicitly reliant on cooperation from fathers to ensure the survival of their offspring,” he says.

Nevertheless, Gettler and others have discovered that parenting behaviour in fathers is accompanied by physiological changes. New dads have lower testosterone levels than men without offspring, particularly if they help with childcare. Fathers of infants also have higher levels of a hormone called prolactin, which may help promote paternal investment in offspring.

This Father’s Day, 15 June, Paul Raeburn enters the debate with the publication of Do Fathers Matter?

Spoiler alert: “they matter a lot,” he writes. Dads influence everything from a child’s social and emotional development to their disease risk. Raeburn concludes that throughout history, societies have downplayed the role of fathers. So much so, that until recently in Western cultures they have even been excluded from the delivery room. He also notes the difficulty of studying paternal care in humans. “We can’t put people in cages, tag them with colourful jewellery, and allow them to mate.”

“ When a babysitting dad gets hungry, he often eats some of his brood”

HAPPY FATHER’S DAY

14 June 2014 | NewScientist | 45

particularly males, a way of adjusting how long they care for the clutch. It’s also a way of recouping some energy,” she says.

This idea seems to be supported by some of nature’s most extreme dads – seahorses and pipefish – 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. Pipefish dads eat, or more accurately absorb, about 20 per cent of their offspring.

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 exclusive male care is the evolutionary default behaviour.

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.

OutnumberedStill, the parenting practices of shorebirds suggest another explanation for devoted fathers – and one that turns Darwin’s thinking on its head. Far from male-based care occurring when females are more common, Tamás Székely at the University of Bath, UK, and colleagues found it had a close relationship with there being an excess of adult males. 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.

Does a biased sex ratio also help explain the parenting style of fish, frogs and invertebrates? It’s likely, but we don’t know yet, says Székely, 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 Székely, answers are most likely to come by thinking big – about what males and females are doing across the whole population. But he acknowledges that this is easier said than done while the behaviour and ecology of the vast majority of animals remain unknown.

We are still far from converging on a unifying theory of fathering – if one even exists. “Personally I don’t believe that there is one correct hypothesis,” says Kokko. But if devoted dads remain a bit of a mystery, we have learned at least one thing since Darwin’s day – being a good father has its benefits. ■

Lesley Evans Ogden is a science writer in Vancouver, Canada. Follow her on Twitter @ljevanso

Jacana dads do everything from nest building to rearing young. Some poison frog dads (left) carry their offspring in mucus backpacks

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“ The parenting practices of shorebirds turn Darwin’s thinking on its head”