Emergency leap after mating

Spider male escapes from cannibalism

Philoponella prominens male jumps away to safety after mating

With a catapult mechanism, a male of the spider Philoponella prominens manages to escape his hungry partner after copulation. Shichang Zhang and colleagues recorded it on video.

For many male spiders, mating is life-threatening. Because to a female, a male not only is a supplier of sperm that she can use to fertilize her eggs, but also a tasty snack. And when he has given his sperm, he is just a meal. Dying without siring offspring is no option. So, he has to proceed with caution, and leave immediately after finishing copulation.

A Philoponella prominens male, a spider species from woods of central China, is very accomplished. After mating, he swiftly leaps away, out of her reach, Shichang Zhang and colleagues show. They recorded mating and leaping with a high-speed camera.

High pressure

During mating, which lasts half a minute, he folds his two front legs against her, the researchers observed. By suddenly stretching them afterwards, he pushes off and shoots away. He had already secured himself before with a safety line of silk, which he had tied to the edge of her web. After leaping, he crawls back via that line to mate with her again. He is able to repeat the action up to six times.

Spiders move their legs not only with muscles, but also use hydraulics. They bend the legs by contracting flexor muscles but lack extensor muscles. Instead, they fill the joints with body fluid at high pressure, so that the legs stretch by released hydraulic power as the flexor muscles are relaxed. In this way, a male Philoponella prominens jumps from his partner. He reaches a speed of about seventy centimeters per second, spinning around at high speed. A female is unable to grasp him.

The leap is lifesaving, as the researchers showed. If they prevented a male from leaping with a fine brush, he was grabbed by his partner and eaten. As if he were just prey.

Willy van Strien

Photo: Philoponella prominens, mala above female. © Shichang Zhang

Emergency leap on video

Another spider male that has to be careful: Maevia inclemens

Source:
Zhang, S., Y. Liu, Y. Ma, H. Wang, Y. Zhao, M. Kuntner & D. Li, 2022. Male spiders avoid sexual cannibalism with a catapult mechanism. Current Biology 32: R341-R359. Doi: 10.1016/j.cub.2022.03.051

Flying saucers

Dance fly female advertises quality by inflating her body

Feamle long-tailed dance fly advertises quality by making herself bigger

Shaped like flying saucers, long-tailed dance fly females seek the attention of males. Their wide shape indicates their quality, Jessica Browne and colleagues write.

Females of the long-tailed dance fly (Rhamphomyia longicauda), which lives in North America, possess ornaments that make them attractive to males. They have sacs on either side of their abdomen and feathery black scales on their legs. By inflating the sacs and wrapping the legs along them while flying, they become laterally expanded. In this way, they show their quality, Jessica Browne and colleagues argue.

Sex roles reversed

In most animal species, females are choosy and males try to impress them by showing off. But in long-tailed dance flies, it is just the other way around: the males are choosy, the females try to seduce them to mate.

The reason is that females are unable to gather their food on their own. They need food to produce eggs, but cannot hunt for the smaller insects on which they live. That is why they have to to be provisioned by males. A male intending to mate brings a prey as a nuptial gift. Females mate frequently, because every mating yields a meal. But males have to catch prey first. That is hard for them, and a male that has gone to all that trouble will offer his gift only to a female that deserves it.

Silhouette

In order to seduce males, females gather in a lek. At dawn or dusk they form a swarm of dozens of flies in a clearing in the forest and ‘dance’ about half a meter above ground level. Males that have captured a prey will approach such swarm from below and see the females silhouetted against the dimly lit sky. Upon detection of an attractive female, a male will hover just below her. She doesn’t miss the chance and immediately drops on him. Together they leave the swarm to mate. She stores his sperm to fertilize eggs with later.

Males prefer large females. To be attractive, females inflate their sacs, lift their legs and wrap them along the laterally expanded sacs, so that their silhouette becomes much wider. They look like flying saucers. The wider a female is, the greater her chance of being chosen.

But what exactly does a large silhouette signify? Why is it beneficial for males to choose such inflated female?

Magnified difference

The higher the quality of a long-tailed dance fly female is, the wider she can make herself, as Browne and colleagues show. A dance fly begins its life as a larva. After pupation, an adult fly emerges with dimensions that are fixed; also the size of the sacs and the scales on the legs of females is fixed. Probably, the size of an adult fly is an indication of quality and a result of how good conditions were during its larval stage. Now, it turns out that the larger a female is, the larger her expandable sacs and leg scales are in proportion. Because large females can make themselves relatively wider, the differences in quality that exist between females are magnified.

Males preferring inflated females are choosing quality.

Paternity not guaranteed

Their choice is a good one, because a wide female potentially produces many eggs. And because she is attractive, she will be chosen frequently and fed many meals, so she will be able to indeed develop those eggs. She also has a good chance of surviving long enough.

But a male that chooses an attractive female can only hope that he will sire some of that progeny. If he is the first to mate her, she will use his nuptial gift to initiate egg development, but by the time she is going to lay them, she has stored sperm from many more males and his chances are small. A male probably has the best chance to sire much offspring if he is the last to mate with her before she starts laying eggs, when they are almost mature.

But in what state of development the eggs of an attractive female are, a male cannot infer from her size. He must be choosy, but he must also be lucky.

Willy van Strien

Photo: Female Rhamphomyia longicauda with inflated sacs. ©Heather Proctor

Sources:
Browne, J.H. & D.T. Gwynne, 2022. Deceived, but not betrayed: static allometry suggests female ornaments in the long‑tailed dance fly (Rhamphomyia longicauda) exaggerate condition to males. Evolutionary Ecology, online Jan. 7. Doi: 10.1007/s10682-021-10148-3
Murray, R.L., J. Wheeler, D.T. Gwynne & L.F. Bussière, 2018. Sexual selection on multiple female ornaments in dance flies. Proceedings of the Royal Society. B 285: 20181525. Doi: 10.1098/rspb.2018.1525
Funk, D.H. & D.W. Tallamy, 2000. Courtship role reversal and deceptive signals in the long-tailed dance fly, Rhamphomyia longicauda. Animal Behaviour 59: 411-421. Doi: 10.1006/anbe.1999.1310

Content with second place

European pied flycatcher may prefer to be a concubine

Female pied flycatcher may become secondary mate of a male

A high quality male is so desirable that a female pied flycatcher may be willing to become his secondary mate – as long as it is not too hard to take care of the young without his assistance, Simone Santoro and colleagues write.

Like most passerine birds, the European pied flycatcher (Fidecula hypoleuca) is mainly socially monogamous. But some males have a secondary female. This concubine gets little help from him when raising the young, but in good years, when food is abundant, that may not be a major problem, Simone Santoro and colleagues argue.

Short breeding season

The males are the first to return from the wintering area in Africa, mid-April. They look for a suitable nest hole, which can be a tree cavity or nest box, and defend a small territory around it. Once a male occupies a good place, he tries to attract a female to breed with. Females visit a number of males before making their choice.

A couple is then busy for about five weeks. She lays five or six eggs and starts breeding when the clutch is complete. Both parents feed the young until they fledge, and dad defends the family. The breeding season covers the months of May and June; only one clutch can be raised in this period. But some males want more.

Good genetic quality

To get more, an ambitious male will have to occupy a second nest site and attract another mate. If successful, he will have to divide his paternal efforts over two nests. The research group, which works in Spain, had already shown how things go.

Males that succeed in starting a second nest are birds that have arrived and started breeding early, and that are able to defend two nests against rivals. These are strong males: of high genetic quality and in good condition. Such male stays with his first mate during the week that she is laying eggs. When she starts incubating, he tries to seduce to a second female. Usually, a second nest is located close to the first one.

When the young hatch in the first nest, he goes there to help feeding them. The primary female gets his full attention. Only when that first nest has fledged does he offer his services to the second nest.

So, the secondary female is worse off, as she has to feed the kids on her own for a while: that is hard work and she will see fewer young fledge. But, on the other hand, these young inherit a good genetic quality from their father. That is why a female may prefer to be the secondary mate of a high quality male rather than the only mate of a low quality male.

Fat and lean years

Particularly later in the season – when desirable single males are not available anymore -the choice to become a secondary female can turn out fairly well, because the time interval between father’s first and second brood will be larger and he will start helping on the second nest earlier.

Now, the researchers show that the availability of food also matters.

Because secondary females have to work harder than females in a monogamous relationship, their chance of survival is lower. (That is also true for primary females. Apparently, the situation is not ideal for them either, but it isn’t their choice.)

However, the lower survival rate of secondary females is an average over years; the researchers followed the birds for 26 seasons. The survival rate varies from one year to the next. In good years, a secondary female has less difficulty raising her young and her chance to survive is almost as high as that of a female in a monogamous relationship. To assess whether a year was good or bad, the researchers considerd the percentage of young that survived and fledged. A good year probably is a year in which food is abundant. In such year, a female can more easily accept a secondary position.

And sometimes. she does, as it turns out: in fat years it is more common for a male to have two families than in lean years. But even then, monogamous relationships remain the majority.

Willy van Strien

Photo: Caroline Legg (Wikimedia Commons, Creative Commons CC BY 2.0)

Sources:
Santoro, S., P. Fernández‑Díaz, D. Canal, C. Camacho, L.Z. Garamszegi, J, Martínez‑Padilla & J. Potti, 2022. High frequency of social polygyny reveals little costs for females in a songbird. Scientific Reports 12: 277. Doi: 10.1038/s41598-021-04423-0
Canal, D., L. Schlicht, J. Manzano, C. Camacho & J. Potti, 2020. Socio-ecological factors shape the opportunity for polygyny in a migratory songbird. Behavioral Ecology 31: 598–609. Doi: 10.1093/beheco/arz220

Hurry up please

Spikethumb frog males transfer messages to females by biting

Spikethumb frog males bite partner during mating

Males of three spikethumb frog species give their mate a chemical message during mating, using their upper teeth, as Lisa Schulte and colleagues show.

During mating, males of some species of spikethumb frogs (Plectrohyla) press their upper lip onto their mate’s head or back. That’s not exactly a caress, on the contrary: they scrape their teeth over it, Lisa Schulte and colleagues found. The scratches are clearly visible afterwards. Why would they do this?

Swollen lips

In three species, females are found that have scratches on their head or back: Hartweg’s spikethumb frog (Plectrohyla hartwegi), Matuda’s spikethumb frog (Plectrohyla matudai), and arcane spikethumb frog (Plectrohyla sagorum). The distance between the scratches is similar to the distance between the upper teeth of the males, which are elongated and protruding. These frogs live in the South American tropics.

In addition to elongated teeth, the males have swollen upper lips during the breeding season. They turn out to contain specialized, large glands. These produce mucus and excrete it on the inside and outside of the lips. The researchers found several proteins in the mucus, including proteins known from salamanders as messenger molecules with which the animals communicate with each other.

Direct message

The conclusion is that during mating, the males transfer the mucus of the glands into their partner’s skin with teeth and lips. These proteins are probably taken up by the blood and delivered elsewhere. As a consequence, eggs are laid more quickly, the researchers think.

That would  be advantageous. When mating, a frog male clings to a female with a mating embrace or amplexus. The two stay like this for hours or even days, until she lays her eggs, and he can fertilize them. And all the while, such a joined pair is less agile than a single frog, and thus an easy prey for predators. The sooner a mating is completed, the shorter that unsafe state lasts.

The males are not very gentle. But if the mating is finished earlier because of the biting behaviour, both partners benefit. It is not yet known whether mating indeed is faster.

Anyway, the males of these frogs give off a chemical message during mating and are sure that it is received.

Willy van Strien

Photo: Plectrohyla sagorum. Ruth Percino Daniel (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Source:
Schulte, L.M., A. Martel, R. Cruz‑Elizalde, A. Ramirez‑Bautista & F. Bossuyt, 2021. Love bites: male frogs (Plectrohyla, Hylidae) use teeth scratching to deliver sodefrin precursor‑like factors to females during amplexus. Frontiers in Zoology 18: 59. Doi: 10.1186/s12983-021-00445-6

Crossdressing in white-necked jacobin

Male-like plumage reduces social harassment in females

in white-necked jacobin, males are brightly coloured

Most white-necked jacobin females are distinguishable from males by a less bright colour. But 20 percent of the females looks like a male. Jay Falk and colleagues wanted to know why they deviate from the normal pattern.

In hummingbirds, a bird family with more than 300 species, males tend to be more brightly coloured than females. But in one in four species, some females have a male-like plumage, as reported earlier this year by the research group that Jay Falk is part of. Now, he tried to figure out why these females dress like a male. He discovered that it enables them to forage relatively undisturbed. They experience less harassment of both conspecifics and other hummingbirds.

most white-necked jacobin females are less colourful than males, but some have male-like plumageThat hummingbird females normally are less colourful than males – though they are by no means dull compared to many other bird species – is because they raise the young. If they are on or around the nest, a dull colour provides safety: their predators detect them less easily. Hummingbird males have no such tasks and are free to seduce females. To be attractive, they have flashy colours, which females like.

White-necked jacobin

But in some hummingbird species, females may have a showy male appearance. The white-necked jacobin, Florisuga mellivora, is an example. About 20 percent of adult females has a shiny blue head, white belly and tail and white spots on the neck like males. Would this confer any benefit?

Perhaps also males prefer a brightly coloured partner, Falk thought at first. But that is not the case, as it turned out when he offered males a choice from several stuffed birds: they prefer a female with normal female plumage.

Harassment

Another possibility is that brightly coloured birds are less likely to be harassed when foraging. Hummingbirds are small animals with a high metabolism that need to consume large quantities of food. So, the birds spend a large part of the day foraging, sucking nectar from flowers. Competition over food is high, and they are quite aggressive around flowers with a high nectar content. Continuously, they are trying to chase each other away.

White-necked jacobin females in female plumage lose out, according to observations. Apparently, they are not impressive. They are more often chased off than brightly coloured animals, both by conspecifics and other hummingbirds. Conversely, they are less aggressive themselves. In addition, they are likely to be sexually harassed more often. Females in male’s outfit, on the other hand, can forage relatively undisturbed.

Accordingly, male-like females were found to visit a place where nectar was offered more frequently than females in female plumage, and they stayed longer. So indeed, male plumage in females is beneficial because it reduces harassment.

A white-necked jacobin female with male plumage does not look exactly the same as a male. When the tail is fanned, a black tail band becomes visible that is wider in these females than in males. They also have some green on the tail.

Brood care

There is another indication that male plumage offers protection against aggression: all young are brightly coloured, while young of animal species usually are camouflaged. Male-like plumage also enables young white-necked jacobins to forage without too much trouble.

So, young females are brightly coloured. As they reach adulthood, 20 percent of females retains that colourful plumage, while the majority, 80 percent, switches to a less conspicuous appearance. Why don’t they all keep looking like males if that increases access to food resources?

Probably because it is still true that during the breeding period a female should not be clearly visible, favouring a less bright colour. Young females don’t have that concern yet.

Willy van Strien

Photos:
Large: white-necked jacobin male. Kathy & sam (Wikimedia Commons, Creative Commons CC BY 2.0)
Small: white-necked jacobin female in female plumage. Joseph Boone (Wikimedia Commons, Creative Commons CC BY-SA 4.0)

Sources:
Falk, J.J., M.S. Webster & D.R. Rubenstein, 2021. Male-like ornamentation in female hummingbirds results from social harassment rather than sexual selection. Current Biology, online August 26. Doi: 10.1016/j.cub.2021.07.043
Diamant, E.S., J.J. Falk & D.R. Rubenstein, 2021. Male-like female morphs in hummingbirds: the evolution of a widespread sex-limited plumage polymorphism. Proceedings of the Royal Society B 288: 20203004. Doi: 10.1098/rspb.2020.3004

Royal matchmaker

Ant worker transports young queen to suitable mates

Cardiocondyla elegans worker carries queen to new nest to mate

Workers of the ant Cardiocondyla elegans make sure that their queen sisters will meet unrelated males, Mathilde Vidal and colleagues show.

Young queens of the ant Cardiocondyla elegans do not leave the natal nest on their own to be inseminated outside. Although they have wings, they make no nuptial flights like queens in many other species. They stay inside. Males have no wings, and they too remain in the natal nest. And so it happens that young queens, or gynes, mate with males that were born in the same nest. But workers intervene to promote outbreeding, Mathilde Vidal and colleagues discovered.

Cardiocondyla elegans, which is mainly found along the Mediterranean, contructs underground nests on river banks. Hundreds of workers, dozens of young queens and a few males share a nest, headed by one fertile queen. This mother queen has mated with several males and stored their sperm to fertilise eggs.

As a consequence, the gynes and males in her nest are full and half siblings. If they mate with each other, this is inbreeding, and prolonged inbreeding has negative effects on the lifespan of mother queens, the survival of brood and the ratio of females (workers and young queens) to males.

Vidal had observed workers walking through the field between nests, carrying a winged young queen on their back. She wondered whether this queen transport could be a way to promote outbreeding. Behavioral observations and genetic research confirmed this idea.

New contacts

The researchers discovered that gynes do indeed mate in the natal nest. But it doesn’t always stop there. A worker regularly drags a young queen out of the nest, takes her head between its jaws and carries her on its back to another nest, where it drops her into the nest entrance.

Just below that entrance, as it turned out, is a chamber with hundreds of young queens and males. It is obvious what is happening there. The nest chambers with mother queen and brood are much deeper, 1 to 2 meters below the surface. By dropping a young queen into the entrance of an alien nest, a worker brings her into contact with males that are not (half) brothers. The nest where a young queen is delivered also profits because males can mate not only with (half) sisters, but also with an unrelated queen.

After delivery, a queen is sometimes picked up again and taken to still another nest.

Hibernation

Young Cardiocondyla elegans queens hibernate in the natal nest or in the nest to which they were brought. They retain their wings. In spring they leave, usually on foot, to found a nest on their own, with a stored stock of sperm from several males: (half) brothers and, if they have been transported to another nest, alien males. Once they have started their own nest, they lose their wings.

Apparently, young queens are able to disperse on their own. Then why don’t they leave the natal nest to mate elsewhere?

Maybe it’s quicker and safer to be carried, Vidal thinks. Workers know the surroundings. Passing by other nests, they walk in a straight line to a nest that they have selected. Often, they will deliver another gyne there later on.

Inhabitants of a preferred nest are no family, so the matchmakers select unrelated partners for their queen sisters. This behaviour is a new and surprising way to promote outbreeding, the researchers state.

Willy van Strien

Photo: Cardiocondyla elegans: worker carrying young queen. ©Mathilde Vidal

Sources:
Vidal, M., F. Königseder, J. Giehr, A. Schrempf, C. Lucas & J. Heinze, 2021. Worker ants promote outbreeding by transporting young queens to alien nests. Communications Biology 4: 515. Doi: 10.1038/s42003-021-02016-1
J-C. Lenoir, A. Schrempf, A. Lenoir, J. Heinze & J-L. Mercier, 2007. Genetic structure and reproductive strategy of the ant Cardiocondyla elegans: strictly monogynous nests invaded by unrelated sexuals. Molecular Ecology 16: 345-354. Doi: 10.1111/j.1365-294X.2006.03156.x

False alarm

Superb lyrebird male tries to prolong a female’s visit

a male superb lyrebirds show is also used to manipulate females

A male superb lyrebird can deceive a female into believing that danger is imminent, Anastasia Dalziell and colleagues think. This increases the chance that she will stay for a while and copulation ensues.

Superb lyrebirds are masters of imitating all possible sounds, and males make clever use of that talent. When a female pays a visit, a male imitates the sound of a flock of alarmed songbirds, creating the illusion that a predator is nearby, Anastasia Dalziell and colleagues write. Then she might stay a little longer than she really wanted.

The superb lyrebird (Menura novaehollandiae), one of the largest passerine species, lives in the forests of South East Australia. Males and females do not form breeding pairs; each bird lives in its own territory. Females have one young per year, which they raise on their own.

Just watching

During the breeding season, males make themselves as attractive as possible. They construct mounds in their territory, where they sing their songs. Sometimes they sing a special song accompanied by a dance according to fixed rules, as Dalziell described earlier, throwing their decorative tail feathers over their body and head.

The purpose of a male’s show, of course, is to attract females and get them to copulate, because every mating can result in a young that he sires. Females visit several males before making their choice. As a result, a female may come to watch a displaying male, but refrain from mating with him in the end.

That is not what he intended.

Illusion of danger

When she is about to leave without copulating, he adds a new element to his song, which is remarkably similar to the sound of a flock of aroused songbirds.

Small songbirds get aroused when they detect a predator, such as a snake, large lizard, roosting owl, or perched hawk. They utter alarm calls to recruit others and harass the enemy together. The researchers show how accurately a male lyrebird mimics such mobbing flock of multiple simultaneously calling birds. Even the noise of beating wings is incorporated into his song. It is so accurate, that small songbirds are misled and approach to join.

The predators that arouse the small birds are dangerous for lyrebirds too. Therefore, the researchers hypothesize, the song creates the illusion that danger is imminent; the female is inclined to stay, and there is a chance that a copulation will happen.

Deception

A male superb lyrebird also utters this cacophony during mating. This job is not done in a few seconds, as it is other birds. Only after havng sat on her for more than half a minute, does he transfer his sperm. From the moment he mounts her until the end, he mimics the sound of a mobbing flock to prevent her from leaving too soon. During mating, he beats his wings in front of him, obscuring her view. She is unable then to assess whether it is safe to go, the authors suggest.

In conclusion, the superb lyrebird male uses his song not only to advertise his good health and condition, as is usual, but also to get a female to stay by giving a false signal of danger. That is deception.

Whether a female will stay longer because of the false alarm, the researchers don’t know. To find out, they would have to do experiments, which would be difficult for this species.

Willy van Strien

Photo: Courting male, covered with his tail. Kim Edol (via Flickr, CC BY-NC-ND 2.0)

Anastasia Dalziell about her research on YouTube

Sources:
Dalziell, A.H., A.C. Maisey, R.D. Magrath & J.A. Welbergen, 2021. Male lyrebirds create a complex acoustic illusion of a mobbing flock during courtship and copulation. Current Biology, online February 25. Doi: 10.1016/j.cub.2021.02.003
Dalziell, A.H., R. A. Peters, A. Cockburn, A.D. Dorland, A.C. Maisey & R.D. Magrath, 2013. Dance choreography is coordinated with song repertoire in a complex avian display. Current Biology 23, 17 juni online. Doi: 10.1016/j.cub.2013.05.018

Sound amplifier

Small tree cricket calls from a window

small tree cricket male calls from a window to amplify its sound

Those that are small must be smart. At least that applies to tree crickets. Males with a softer call than others have an effective strategy to amplify their sound, as Rittik Deb and colleagues show.

Small crickets face a problem. To attract females, cricket males raise their forewings and rub them together. The forewings are leathery and provided with a comb. The rubbing causes them to vibrate, and as vibrating membranes, they produce sound waves: the familiar chirping. But at the wing edges, the sound waves are attenuated, softening the sound. Especially for small species, with small wings, that effect is significant. For instance for tree crickets (Oecanthus species), with wings only about one centimeter long.

Small and soft calling males of tree cricket Oecanthus henryi, which lives in India, have a unique method to amplify their sound, Rittik Deb and colleagues report: they turn a leaf into a sound amplifier.

Pear-shaped hole

The chirping noise is extinguished at the wing edges because waves at the front and back side are in opposite phase. That is because when air is compressed by the vibrating wings at the front side (creating a wave peak), it expands at the back (wave trough) and vice versa. At the edges, waves cancel each other out because of these opposite phase, resulting in a softer sound.

Tree cricket males can prevent this by separating the waves from the front and back side with a baffle. They do this by cutting a small window in a leaf and taking place in it to sing, with the head directed to one side, the abdomen to the other, and the raised forewings perpendicular to the body, in the plane of the leaf.

Previously, the researchers had shown that tree crickets can create a nearly perfect window in one go. They make such hole only in larger leaves of their host plant, Hyptis suavevolens. That makes sense, because large leaves produce a clear effect. The best place for the hole is in the center, but there the midrib runs. The leaf would wither when the tree crickets pierced it. So, they cut the hole close to the center, next to the midrib. And they make the hole pear-shaped, fitting the male with raised forewings, with the edges of wings and window close to each other.

The baffle is a good sound amplifier. The call is louder than it would be without it. For females, this is more attractive. In addition, the sound travels further, reaching more females.

More sperm

Yet not all tree cricket males take the effort to make such sound amplifier. Now, the researchers show that mainly the smaller ones with a soft sound do it, and explain why they do it.

By singing with a self-made baffle, small and soft calling males increase females’ attendance, as expected. With this sound amplifier, they may attract about six times as many females per night as without baffling, the researchers calculated. That is a considerable gain. Large and loud calling males can attract more females with a baffle too. But it doesn’t help them much, because even without sound amplification, they get as many mates as they can handle. They do not need to attract more females.

Large and loud males therefore call in the standard way: from the edge of a leaf. But other males make a window to amplify the sound of their call. This makes them appear larger than they really are, and females are misled. They mate longer with louder calling males – either large males or small, baffling ones – so that these males can transfer more sperm. By making a baffle, small and soft calling males increase their reproductive success, which would otherwise be quite low.

Willy van Strien

Photo: Oecanthus henryi. ©Rittik Deb

Sources:
Deb, R., S. Modak & R. Balakrishnan, 2020. Baffling: a condition-dependent alternative mate attraction strategy using self-made tools in tree crickets. Proceedings of the Royal Society B 287: 20202229. Doi: 10.1098/rspb.2020.2229
Mhatre, N., R. Malkin, R. Deb, R. Balakrishnan & D. Robert, 2017. Tree crickets optimize the acoustics of baffles to exaggerate their mate-attraction signal. eLife 6: e32763. Doi: 10.7554/eLife.32763

First amiable

Older painted turtle male switches to violent behaviour

painted turtle male is amiable until he gets older

During their life, painted turtle males change their behaviour towards females. They switch from courtship to coercion, Patrick Moldowan and colleagues witnessed.

Mating is often a pleasant affair in the painted turtle, Chrysemys picta. A male courts a female and at one point he strokes her head with his fore claws, which are elongated in males. If she is receptive, things go on. This state of affairs was known.

But males are not always that friendly, according to Patrick Moldowan and colleagues, who study the animals in wetlands in Canada. They had noticed that during the breeding season, in late summer, many females have bite wounds on head and neck. Apparently, males can become outrageous and bite, they write. They wanted to know more.

Claws or teeth

As it turned out, the tactic with which a painted turtle male approaches a female depends on his size, and thus on his age. The researchers discovered this by temporarily enclosing animals, after measuring their size, in a cage in their living environment. They videotaped their behaviour and watched the footage afterwards. Young adult men are gallant lovers, they saw. Their fore claws are very elongated. But as males get older and grow, their fore claws don’t. As a result, they are getting smaller in proportion.

At the same time, males develop ‘weapons’. Two tooth-like cusps (tomiodonts) appear at the front of the upper jaw. In males, those teeth are much more prominent than in females, and when a male grows, his teeth get proportionally larger. In addition, projections develop on the anterior edge of his upper shell. Males use these weapons to force women into mating; they bite and they clatter with their shells.

So, males switch from a friendly to a violent attitude towards females during their lifetime; the relative size of claws, tomiodonts and carapace projections matches their behaviour.

Storage

A successful mating can result in many offspring; also in the long term, because a female stores the sperm for a long time. It therefore makes sense that a painted turtle male strives to get access to a female. But why do only small males this in a kind way? Perhaps because females, that are larger on average, would be able defend themselves well against unfriendly small males. It’s then better to be nice. But as males get bigger and stronger, coercion appears to be more successful.

Unfortunately, the researchers could not see whether large males were really able to enforce mating, because the animals didn’t go so far during the experiments.

Willy van Strien

Photo: Rickard Holgersson (via Flickr, Creative Commons, Public Domain)

Sources:
Moldowan, P.D., R.J. Brooks & J.D. Litzgus, 2020. Sex, shells, and weaponry: coercive reproductive tactics in the painted turtle, Chrysemys picta. Behavioral Ecology and Sociobiology 74: 142. Doi: 10.1007/s00265-020-02926-w
Moldowan, P.D., R.J. Brooks & J.D. Litzgus, 2020. Demographics of injuries indicate sexual coercion in a population of Painted Turtles (Chrysemys picta). Canadian Journal of Zoolology 98: 269-278 Doi: 10.1139/cjz-2019-0238
Hawkshaw, D.M., P.D. Moldowan, J.D. Litzgus, R.J. Brooks & N Rollinson, 2019. Discovery and description of a novel sexual weapon in the world’s most widely-studied freshwater turtle. Evolutionary Ecology 33: 889-900. Doi: 10.1007/s10682-019-10014-3

Males parasitizing on females

The immune system of deep-sea anglerfishes is strongly modified

In deep-sea anglerfish, some species have parasitic males and an aberrant immune system

To the well-known peculiarities of deep-sea anglerfish, Jeremy Swann and colleagues add a new one: some species lack an important part of the immune system. This is associated with a unique parasitic lifestyle of males.

There are strange, very strange and extremely weird animals. We can safely include deep-sea anglerfish in the latter group.

Within the anglerfish or seadevils, they form a separate group of over 160 species, the Ceratioidea, which, as the name indicates, have specialized in living in the utter darkness of the deep sea. Food and partners are extremely scarce down there. Hence, as was known, these fish exhibit some peculiarities. Now, it turns out that they also have a very aberrant immune system, Jeremy Swann and colleagues report.

Angling pole with glowing bulb

Deep sea anglerfish start their lives in a quite normal way, eggs and larvae dwelling in surface waters. But once they developed into young fish, things change. Females grow to a considerable size, males stay tiny.

The bigger a female gets, the more eggs she can produce. And so a young female starts growing. She has to eat much, several prey animals are on her menu. To capture prey, she uses a fishing rod growing from her back; it is a modified anterior dorsal fin. At the end it has a lure: a bulb in which bacteria live that produce light by carrying out a chemical reaction. It is a form of mutualism; the bacteria get a place to live in and food in exchange for light production.

An anglerfish’s light can flash and dance, resembling a moving animal. Living animals discern a tasty snack which they will approach. The anglerfish then ingests a large amount of water, including prey. With some luck, the catch will provide sufficient nutrients to sustain her for quite a while.

The females, plump and with large heads and mouths full of sharp teeth, are not the prettiest of all. They are called seadevils for good reason. They are bad swimmers, drifting around, just waiting for prey to come by.

Strong attachment

After completing the larval stage, males’ development takes a completely different direction. Males no longer grow and are unable to eat. Their only goal is to find a female in the empty deep sea. So, they swim constantly. In addition to the light bulb of their angling rod, young females also have two luminous organs on their backs. Maybe the dwarfed males, which have big eyes, are able to detect those organs. If they are lucky, they will meet a partner before they have used up all their reserves.

Upon meeting, he attaches himself to her body with sharp teeth. When, later on, she is ready to release eggs, he is ready to fertilize them. Males and females only become sexually mature when they’ve acquired a partner. Given the scarcity of conspecifics, this makes sense: only after pair formation it is guaranteed that eggs and sperm can come into contact.

Sperm bulge

In some deep-sea anglerfish, the attachment between female and male is temporary; after a while, he lets go.

But in other species, males attach themselves permanently to a female. These are most bizarre types, because the two partners fuse with each other, enabling the male to survive. Their skin tissues meld, the circulatory systems become connected. He now is a ‘sexual parasite’, little more than a sperm-producing bulge that feeds on nutrients that he derives from her. This sexual parasitism is a unique mode of reproduction, occurring only in deep-sea anglerfish.

It is called parasitism, but it may be considered a form of mutualism as well, as the male delivers sperm in return for nutrients.

The best known species is Ceratias holboelli; it is also the largest one and it has the most extreme sexual dimorphism. A female can grow more than a meter long (including tail), sixty times the size of a free-living male. Physical pair formation is permanent. Once attached to her belly, he grows to a maximum of 20 centimetres. A female carries no more than one parasitic male.

Another species with permanent attachment is Cryptopsaras couesii; in this species, up to eight males can be attached to a single female. A female can be 30 centimetres long, a free-living male only three centimetres.

Ancient immune system

It is remarkable that the female immune system doesn’t attack permanently attached, parasitic males, Swann and colleagues realized. You would expect the immune system to recognize and reject such males, as they are not-own tissue. But that does not happen.

Apparently, the immune system tolerates the very intimate mode of reproduction. To find out how, the biologists examined a number of genes that underpin various parts of immune defence. They investigated four deep-sea anglerfish species with temporarily attached males and six species with permanently attached parasitic males, including Cryptopsaras couesii. They compared these species to a number of anglerfish species outside the deep-sea group, where males don’t attach to females.

Fishes have the same immune system as other vertebrates; the system is 500 million years old. It consists of innate, general immune responses on the one hand and specific immune responses that build up against specific intruders that the system has to deal with on the other hand. The researchers focused on the adaptive, specific immune system.

Lethal

The results were surprising: deep sea anglerfish species in which males live as parasites on females lack essential immune genes. Their specific immune system is severely blunted.

In two of the species studied, species in which females can have more than one male attached, virtually no specific immune facilities are functional. This is highly remarkable, because such complete lack of specific immune defence is lethal for other animals. The first infection would kill them. Microbial pathogens occur in the deep sea too, so deep-sea anglerfish must be able to defend themselves. Most likely, they reorganized their innate immune defence, the researchers assume.

From their own and other research, they conclude that the common ancestor of deep-sea anglerfish had tiny, non-parasitic males that temporarily attached themselves to females. On a few occasions, species descending from that ancestor made the switch to permanent attachment and their specific immune defence has been largely dismantled.

It is unclear yet what happened first. Did males become parasitic, making it necessary to turn off the specific immune system? Or did the specific immune system lose important parts, making permanent attachment of males possible?

The deep sea anglerfish remain really puzzling creatures.

Willy van Strien

Drawing: northern giant seadevil, Cryptopsaras couesii (not included in this research); female with male attached. Tony Ayling (Wikimedia Commons, Creative Commons CC BY-SA 1.0)

Watch the fanfin angler, Caulophryne jordani (not included in the research) on YouTube; female with permanently attached male

Sources:
Swann, J.B., S.J. Holland, M. Petersen, T.W. Pietsch, T. Boehm, 2020.  The immunogenetics of sexual parasitism. Science, online July 30. Doi: 10.1126/science.aaz9445
Fairbairn, D.J., 2013. Odd couples. Extraordinary differences between the sexes in the animal kingdom.  Princeton University Press, Princeton and Oxford, VS. ISBN 978-0-691-14196-1