CHAPTER 2

Six-legged Sex: Dating, Mating and Parenting

What accounts for the enormous success of insects as an animal group? Why are they so rich in species and why are there so very many of them? Put simply: because they are small, supple and sexy.

Life on our planet spans more than 10 orders of magnitude – from mycoplasma bacteria (measurable in nanometres) to the gigantic redwood trees of California, which can grow to heights of more than 100 metres. Insects can be found in six of these, all at the lower end of the scale – from wingless male fairy wasps, which are smaller than the cross section of a human hair, to stick insects the length of your forearm (see here). In other words, most insects are small, so they need only a tiny place to hide from their enemies and can exploit resources that are of no interest to larger creatures.

Insects are also unbelievably supple – in the sense that they are flexible and adaptable. Their wings allow them to disperse over areas that are extremely large in relation to their modest size, and their mastery of the three dimensions of airspace gives them access to a great many more sources of nutrition. The fact that most insects spend their childhood in a body shape totally different to their adult form (see here) means that they can exploit entirely different habitats and sources of food in the different stages of their lives – and the young do not compete with the adults for food.

Last but not least, insects have an astonishing capacity for reproduction. There must surely have been a fly on the wall who thought God was talking to her when He said ‘Be fruitful, and multiply, and replenish the earth and subdue it!’ (Genesis 1:28, New King James Version). Just listen to this: take two fruit flies and leave them in ideal living conditions for a year – equivalent to 25 generations for fruit flies. Every fruit fly mother lays 100 eggs. Let’s say that they all grow to adulthood, and that half of them are females who mate and lay another 100 eggs. Once the year is over, you will be left with the 25th generation and that alone will amount to almost a tredecillion sweet little red-eyed fruit flies. A tredecillion is the figure 1 followed by 42 zeros. To make this figure more meaningful, imagine packing these flies together densely, as densely as possible, into one enormous fruit fly ball. You’d end up with a sphere whose diameter exceeded the distance between the Earth and the sun! It’s a good thing these insects have so many enemies because otherwise there wouldn’t be any room left on Earth for us humans.

Fortunately (we might say) most of the insect eggs will never catch so much as a glimpse of adult life. Most insects starve to death, are eaten or die in some other way long before they start a family. It’s a harsh struggle. Over time, an incredible range of adaptations has come about, especially when it comes to choice of partner and propagation. We will look at some of them in this chapter.

50 Shades of Strange

Insects’ senses are crucial to their quest to find a partner, and the competition here is tough. But the struggle is far from over when boy meets girl. On the contrary, it has barely begun, because the question of how to pass on as much of their genetic material as possible may have different answers for the two sexes. For example, it’s not unusual for the female to mate with several males over a short period, and the male takes a dim view of this because it means that his sperm face competition. Consequently, many insects come equipped with a male sex organ reminiscent of a Swiss Army knife, complete with all sorts of imaginatively shaped scrapers, ladles and spoons. The purpose? To eliminate any sperm that got there before their own.

This toolkit also comes in handy if the previous male has resorted to another trick: plugging up the female’s genital opening. The idea is to create a kind of homemade chastity belt that prevents the female from being able to mate again. The gambit is only partially effective, as male number two simply uses his scrapers, pike poles and hooks to remove the bung and gain access for his own equipment. So much for candlelight and tender caresses!

Another trick the male deploys is to ensure that as much of his sperm as possible is delivered to the female, and that she has as little time as possible available for other males. He does this by making their mating process as lengthy as possible. Some species take this to extremes: the Southern green shieldbug, Nezara viridula, which has spread all over the world, including to the UK as a stowaway on imported foodstuffs, can keep at it for 10 whole days. And that’s still nothing compared with Indian stick insects, which have apparently been known to stay stuck together for an insane 79 days in an extreme sport version of tantric sex!

As well as engaging in prolonged mating, the male often keeps an eye on the female post-consummation. Have you ever seen those small blue damselflies, a close relative of the dragonfly, perching or flying around in pairs? Sometimes the coupling creatures resemble a heart – although that doesn’t imply any human notions of romance. The sole purpose of this tandem position is that it allows the male to keep watch on the female and make sure she doesn’t mate with any rivals until she has laid (what he hopes are) their jointly fertilised eggs on a suitable aquatic plant.

© Carim Nahaboo 2019

These highly demanding competitive conditions make it vital to keep your equipment in order. And the tiny fruit fly Drosophila bifurca is one insect whose equipment is beyond reproach. This little critter, a close relative of the same fruit flies that drive you crazy in your kitchen, is the proud holder of the record for the world’s longest sperm: at almost 6 centimetres long, it is 20 times longer than the creature itself. For men, that would be equivalent to having sperm the length of a handball court! How is it even possible?

The answer is that the whole thing consists largely of a thin tail bundled up into a ball. Enlarged photographs of the sperm look a bit like what happens when the kids make dinner and forget to put enough water in the spaghetti pan. So, what’s the point? Well, the long sperm are the fruit fly reproductive system’s answer to Usain Bolt: the longest sperm outcompete the shorter and are more likely to win the race to fertilise an egg.

And since we’re in the realm of the bizarre, there’s no getting away from bedbugs – those blood-sucking rascals that hide out in cracks in the wall and beds in flats and hotels the whole world over. When darkness falls, out they shuffle to poke their sucking snouts into you as you sleep. They’re definitely not the kind of souvenir you want to bring back from your holidays, but the fact is that bedbugs are a growing problem, all over the world. In part this is because we travel a lot, but the main reason is that bedbugs have developed resistance to the most common insecticides, so that they no longer kill them.

At any rate, the point in this context is that the males of certain true bug species, including bedbugs, skip anything resembling foreplay; they can’t even be bothered to find the female’s genital opening but simply stick their sex organ into her belly and leave the sperm to find their way through the orifice to the egg cells. This often injures the female, preventing her from being able to mate with any other partners. In this way, the male attempts to ensure that he will be the father of her child. That said, the female has evolved a reinforced area on her belly where the male most often punctures her, which limits her injuries. This illustrates an important point: the battle of the sexes involves two warring parties and both sexes fight for what is most advantageous to them from an evolutionary point of view.

Ladies’ Choice

It’s possible that early insect researchers, almost exclusively men, tended to see everything from the male perspective. Be that as it may, the fact is that modern research yields ever more examples of how female insects also work to advance their own interests.

One such example is the way certain females simply gobble up the male once they’ve finished mating. This is most common among spiders, distant relatives of insects. The male American fish spider, for example, dies in the middle of the act. This is because his sex organ bursts once he’s delivered his sperm (or to put it in dry scientific terms: ‘We observed that mating results in obligate male death and genital mutilation’). And then he gets eaten – for the sake of the children. Even though his chosen one is a chubster 14 times his weight, his little body still provides a useful protein boost. A little extra food comes in handy when you’re preparing to lay hundreds of spider eggs.

The praying mantis is also famed for what is known as sexual cannibalism. That said, field studies have demonstrated that the male ends up on the supper menu more rarely when he mates in natural surroundings than in artificial, laboratory conditions. However, the insect mum has plenty of other tricks up her sleeve: it turns out that she can secretly control which males get to father her children. A great many mechanisms come into play here; the sperm’s quest to reach the egg is more like an obstacle race than a gentle dip in calm waters. Since it is common for the sperm to be stored in a special ‘sperm bank’ inside the female, for the actual fertilisation of her eggs to happen at a later stage she has several ways of influencing which sperm to save and use.

One scientist carried out a cunning if brutal experiment to demonstrate this. She split a pile of flour beetles into two groups. Half the males were put on a starvation diet to make them look like weak specimens with poor genetic quality. Of the females, the scientist simply killed half so that they couldn’t influence the outcome. When the scientist put the beetles together, both the starved and the well-fed males mated away with living and newly defunct females, of which there were equal numbers. And now the really clever bit: the scientist found that the internal sperm banks of the dead females contained just as much sperm from the hungry, poor-quality males as from the well-fed, high-quality males. Those of the living females, however, contained a great deal more sperm from the high-quality males. This indicates that the female was taking active measures to control the whole process and ensure that the strong, high-quality males would father her children.

Life Without Men?

There are plenty of ways to solve the conundrum of ensuring that ‘generation shall follow generation’, and insects offer several examples of most options. Sexual reproduction, which requires both a male and a female, is the most common – among insects too. But many insects can opt for the single life and still continue their line. In fact, several insects are periodic practitioners of virgin birth. Female aphids, for example, can use this method to achieve a quick, effective baby boom on your rosebush in the spring. They don’t have time to hang around and wait for their eggs to hatch, so they simply give birth to living aphid babies, from egg cells that develop into new individuals without being fertilised. And that’s not all: in some aphid species, the females can be like Russian dolls – they contain baby aphids that are themselves already carrying new female aphids!

No wonder your rosebush is teeming with life! Despite the absence of men, it’s questionable whether we can accurately call this ‘the single life’. Soon there won’t be enough room for all of them on the same bush. Up until now, the ladies have been wingless but now it’s time to squeeze out a few winged females who can fly over to the neighbouring bush and continue the mass production there.

When the days grow shorter, the temperatures fall and autumn is on the way, another change is triggered. The aphid ladies switch to production of males and females. These then mate and this time the female lays eggs – the only way that aphids can survive the winter. She places her eggs on a suitable perennial plant. When spring comes, the eggs will hatch new virgin-birthing females. And the game is on again.

So why is there actually any need for men if, in a single season, an aphid lady can be sole progenitor of more children, grandchildren, great-grandchildren and so on than there are humans on the planet? Wouldn’t it be more productive if all individuals were able to produce offspring rather than just half of them? (Not to mention all the time saved if there were no need to worry about dating . . .)

Biologists have long been interested in the question of why most animals and plants come in two sexes, and the discussion is still ongoing. One disadvantage with virgin births is that all the individuals are genetically identical, which leaves species less room for manoeuvre if environmental conditions happen to change. Consequently, sexual reproduction, which blends the genetic material of two individuals, is a good and necessary means of promoting genetic variation and weeding out harmful mutations. Another handy thing about having two sexes is that it also allows species to rely on different strategies: one sex may have few but large and nutritious sex cells – egg cells – while the other may have many small mobile sex cells – sperm cells.

Long Live the Queen!

Aphids aren’t the only insects who live in a thoroughly female-dominated society. It is extremely likely that every single ant, stinging wasp and honeybee you’ve ever seen was female. With very few exceptions, at any rate.

Do you remember Bee Movie, the film about Barry, the male bee who gets bored of life as a factory worker in the beehive? Biologically speaking, it’s all wrong. So, for that matter, is Shakespeare’s Henry V, in which he describes how the many inhabitants of the beehive are overseen by a bee king. The worker bees in the beehive aren’t males, nor are they ruled by a king bee.

The ladies are the ones who decide and do all the important work in the world of the honeybees. All the worker bees are female and their ruler is a queen. The males, the drones, only live for a short period in the autumn and have just one role: to mate with a new queen. The male bees don’t even gather their own food but are fed by the female workers.

Now perhaps we can forgive Shakespeare, DreamWorks, and the other people who have got this so badly wrong, as the misconception is old and hard to put to rest. The Ancient Greeks tried to find out about the lives of bees but just couldn’t get it all to add up. After all, they knew that normal honeybees had stings – and surely women couldn’t come equipped with such a formidable weapon? And if the short-tempered stingers were women then the large, sluggish individuals who couldn’t even be bothered to collect nectar must be men, and that just couldn’t be the case, could it?

It wasn’t until the end of the 1600s, when microscopes came into use in dissection, that it became possible to establish that, yes, the tireless, terrifying workers and their monarch were all women, and the idlers were men. But it would be another 200 years before people truly understood how bees came into the world, because nobody had ever seen a honeybee having sex. The prevailing theory in those days was that the male bees, the dozy drones, engaged in the whole process at a respectful distance, remotely fertilising their queen with what was fancifully referred to as ‘sperm odour’.

Only in the late 1700s was it discovered that queen bees who had been out for a flutter returned to the hive with a male sex organ attached to their own genital opening. These are the remnants of the lucky winner, selected from a swarm of drones who have chased her. The queen often mates with several members of the swarm. She saves up all the sperm cells (as many as 100 million) in a special internal sperm bank and doles them out as needed over the rest of her life.

For the drone, however, mating is the last thing he will do with his life. The actual transmission of sperm is nothing short of an explosion – so powerful that the drone’s sex organ splits open and is torn loose from his abdomen, and he dies shortly afterwards. A bit like a miniature version of ‘comes in like a lion, goes out like a lamb’. It’s so extreme that it has even inspired the tabloids to devote a few column inches to insects, accompanied by headlines like this one from The Sun: ‘Male bees’ testicles EXPLODE when they reach orgasm’.

Beyoncé Was Right

From the bees’ queen to the woman today’s music fans call Queen B – American pop diva Beyoncé Knowles. Insects got a PR boost from an unexpected quarter a few years ago when media platforms worldwide broke the news that a new species of horsefly had been discovered and named after Beyoncé: Scaptia beyonceae.

There are two reasons why the Beyoncé horsefly got its name: first, because it was originally collected in 1981, the year of her birth, although it wasn’t confirmed or named until long afterwards; secondly, and more importantly, because it had such a beautiful backside. The trimming of golden hairs on its rump reminded the scientists tasked with naming the species of the artist’s own rear end when encased in tight, glittering diva dresses. (I eagerly await the day when there are more of us women entomologists, so we can start naming insects for their broad, manly winged shoulders or their ripped abs . . .)

I’m not sure how flattered Beyoncé was, if indeed she was even aware of the whole business, considering that the horsefly concerned was from inland Australia. Although horseflies are flower visitors and contribute to pollination, they are primarily known as nuisances to people and domestic animals; it hurts when they take a chunk out of us, they stress animals out and they can transmit disease. At any rate, around the same time as all this was going on, Beyoncé had a major hit that asked the question: ‘Who run the world?’ Perhaps you know the answer: girls!

I don’t think for a second that Beyoncé had insects in mind when she sang this. But she might just as well have done. Because if we count up all the male and female animals on the planet, insects are responsible for ensuring that there are more girls on Earth. If we ignore bacteria, hermaphrodites and other organisms without any clear gender and study the proportion of females among the remaining animals, some extremely abundant groups, such as insects, are notably dominated by females. The honeybee workers are women, all 83 billion of them. All ant workers are women, and there are enormous numbers of ants on planet Earth; although there is no agreement over an exact figure, the BBC believes it is safe to assume that ants are the most abundant type of insect on the planet. And other fairly abundant insect species, such as aphids, may be female dominated at certain times of the year (see here).

Could this female domination on land be offset by aquatic species? The sea contains small crustaceans, the aquatic counterparts of insects, which dominate in number terms – creatures like Calanus finmarchicus and other types of copepods. The sex distribution among these is more equal, but in this group, too, scientists sometimes report an excess of females. Even among farmed cattle and poultry, which have a large presence on the planet, bulls and roosters are normally outnumbered by their female counterparts. Okay, there are also some organisms that typically have an excess of males, including some flatworms and tortoises, but it is unlikely that this is enough to help correct the imbalance. So, it looks as if Queen B was right in a way. Calculated by the number of total individuals, ‘girls’ really are the ones who make the world go round, thanks to insects and the extreme dominance of females in the most successful species.

I Am Fatherless but Still Have a Grandfather

How can social insects such as honeybees, ants and many wasp species form societies with such skewed sex distribution? Part of the secret lies in how the sex of the offspring is determined in these insects. For human beings and many other insects, sex chromosomes determine the whole business, but these kinds of insects don’t have sex chromosomes.

Sex is determined by whether the egg is fertilised or not – and the queen is the one to decide that. She’s the only one allowed to lay eggs. If she fertilises the egg with the sperm she has saved up from the swarming, it becomes a female – a worker or a queen, depending on the nourishment it receives during the larval stage. If she lays an unfertilised egg, it becomes a male.

This system leads to some genetic peculiarities, especially if the queen has only mated with one male in her life. Because in that case, the queen’s daughters will be more closely related to their sisters than to any offspring they themselves might have! Put simply, this is because every one of the bee dad’s sperms contains exactly the same genetic material, so all his daughters (he cannot have sons – remember, they only develop from unfertilised eggs) inherit identical genes from him. This makes it more advantageous for these daughters to opt out of having children themselves and instead help feed up more sisters, including new queens, simply because that strategy will enable them to pass on more of their own genetic material.

For a long time, people thought this provided a good explanation for the social insects’ strange societies dominated by sterile workers, but we now know that honeybee queens usually mate with several males. And in termites, which are also social, sex is not determined by whether or not the egg is fertilised – so that explanation simply doesn’t hold up. Impassioned debate continues over what other mechanisms might explain the phenomenon. At any rate, this strange system means that some unexpected challenges would arise if a male bee tried to draw his family tree. After all, he has no father, since he was born from an unfertilised egg. Yet he does have a grandfather, a maternal grandfather to be precise. Our human hobby of genealogy – involving my children, your children and our children – is a piece of cake by comparison!

Parental Leave the Insect Way

Insect mums generally consider their job to be done and dusted once the egg has been laid. But there are exceptions. Some insects are genuinely nurturing, providing variants of both bottle feeds and nappy changes. And these discoveries are incredibly useful beyond providing material for your next dinner party anecdote. By studying strategies used by related species that do and don’t engage in childcare, or by manipulating species and observing the impact on the offspring’s survival, biologists have learnt a great deal about ecology and evolution.

For example, there is a cockroach (Diploptera punctata) that gives birth to living young. This means that the eggs hatch inside her, so the nymphs must be fed some nutrients in order to grow up big and strong. Cockroaches don’t have a warm, cosy uterus where their young are fed intravenously through an umbilical cord. Instead, the mother has special glands in her abdomen that excrete milk protein in liquid form. The nutritional content of this ‘milk’ is supposedly like battle rations – an optimal blend of proteins, carbohydrates and fat. Some claim it could become the new superfood for us humans too, but since it’s pretty time-consuming milking cockroaches, we’ll probably have to opt for producing the milk synthetically.

Another of our less popular insects, the deer fly, has a similar life cycle. A parasite that sucks deer blood, it swarms at the height of the mushroom-picking season. Although it rarely stings humans, it is annoying when masses of them land on you, shed their wings and crawl around in your hair. But for elks, they are a genuine problem. One elk that was examined by Norway’s Veterinary Institute in 2007 was found to be infested with 10,000 deer flies.

Deer-fly eggs also hatch inside the mother and the fly larva is ‘breastfed’ through special glands inside the maternal body, while the mother sits snugly ensconced in the elk’s fur. Her offspring are ‘born’ in the form of a sort of pupal cocoon, which becomes hard and black as an ebony bead, then falls off the elk and onto the ground. There it lies until it hatches the following autumn, when the cycle starts again.

Other insects also nurse and nurture their young. We have already taken a look at the social insects, where all the many sisters are employed as nannies for their younger siblings. And their mum is far from lazy, either. A termite queen drops a new egg every third second throughout her entire life so it’s no wonder she needs help from their older siblings

Earwigs, those elongated brown insects with a pincer at the rear, are particularly affectionate mothers. While they may not exactly change nappies, they do keep watch over their eggs, cleaning away fungus spores and washing them with a substance that is assumed to inhibit the growth of mould and fungus. When the young first hatch, she fetches food and feeds the small nymphs. An experiment showed that earwig mums’ tender care multiplied the eggs that hatched from 4 to 77 per cent. Sexton beetles are another example of caring parents (see here).

And it’s not all about the mothers. In Scandinavia, we are proud of our progress on the gender equality front. But when it comes to the smallest among us, other countries are streets ahead on this issue – maybe because there isn’t a single representative of giant water bugs (Belostomatids) in Norway. Also known as toe-biters and electric light bugs, this subfamily contains a rare example of fathers being the ones who take parental leave. In fact, they take on a whole brood, from different mothers. After mating, the female lays her eggs in neat rows on the father’s back, and it’s his job to look after them, floating on the surface of the water and making sure that the eggs neither dry out nor drown. And the mother? Like Ibsen’s Nora, she goes her own way.

Some insects will go to extreme and savage lengths to raise their young. Not by sticking around to look after them, but rather by making sure there is fresh meat waiting when the larva hatches – by placing the egg inside another living being. In the next chapter, we will look at some of the strange ways insects eat – and are eaten.