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

Tap dance

Courting blue-capped cordon-bleu stamps its feet while bobbing

Blue-capped cordon-bleu performs tap dance

In blue-capped cordon-bleu, male and female show their commitment with song and movement. With a high-speed camera, Nao Ota revealed the tap dance that is hidden within.

The complex courtship displays of the blue-capped cordon-bleu, an estrildid finch species from East Africa, are nice to observe. Holding a piece of nesting material in the beak, the bird is singing and bobbing up and down. What we don’t see is that it rapidly stamps its feet several times during bobbing. Nao Ota made that ‘tap dance’ visible by recording the courtship with a high-speed camera. Earlier, she had filmed birds in the lab, now she also has footage from the field.

The birds live in monogamous pairs. Male and female look similar, but the male has more blue plumage than the female. Both sexes give song and dance performances.

Commitment

Blue-capped cordon-bleus perform most intensively when their mate is present on the same perch, but they don’t perform a duet. In contrast to humans, they may be able to see the fast tapping. Feet stamping produces sound, as Ota had already shown, and the birds probably feel the vibrations it causes in the perch on which they are sitting.

In presence of a conspecific bird besides the couple, they sing and dance more frequently. The performing bird then points its tail towards its mate. This seems to mean that the display is directed to the partner and to express commitment.

Willy van Strien

Photo: Blue-capped cordon-bleu, Uraeginthus cyanocephalus, male. Peter Steward (via Flickr. Creative Commons CC BY-NC 2.0)

Hear the song and watch the tap dance on YouTube

Sources:
Ota, N., 2020. Tap dancers in the wild: field observations of multimodal courtship displays in socially monogamous songbirds. The Science of Nature 107: 30. Doi: 10.1007/s00114-020-01686-x
Ota. N., M. Gahr & M. Soma, 2018. Couples showing off: Audience promotes both male and female multimodal courtship display in a songbird. Science Advances 4: eaat4779. Doi: 10.1126/sciadv.aat4779
Ota. N., M. Gahr & M. Soma, 2017. Songbird tap dancing produces non-vocal sounds. Bioacoustics 26: 161-168. Doi: 10.1080/09524622.2016.1231080
Ota. N., M. Gahr & M. Soma, 2015. Tap dancing birds: the multimodal mutual courtship display of males and females in a socially monogamous songbird. Scientific Reports 5: 16614. Doi: 10.1038/srep16614

White bellbird is the noisiest

Female runs a risk of hearing damage

White bellbird sings the loudest call

To seduce a female, a male white bellbird calls out to her so loudly at close range, that she may suffer hearing damage, Jeffrey Podos and Mario Cohn-Haft think. Still, she has to expose herself to the deafening noise.

Not all songbirds have a pleasant song. There are also squeakers, males that call as loudly as possible. Their call definitively is impressive. Up to now, the South American screaming piha, which emits an ear-splitting lashing sound that is characteristic for South-American rainforest, held the record for the loudest bird call.

But now, it turns out not to be the noisiest; it is surpassed by the white bellbird from the northeast of the Amazon. Its call can be three times as loud as that of the screaming piha, Jeffrey Podos and Mario Cohn-Haft discovered. The song consists of two tones and sounds like a horn.

Males of screaming piha and white bellbird do not invest time in raising their young; breeding and feeding are females’ tasks. Males are free and try to mate as many females as possible. To outdo each other in attractiveness, they scream, often in loose groups.

The screaming piha relies completely on its vocalization, as it has a dull appearance. But in the white bell bird, the eye also is to be satisfied. The males are white and have a long black fleshy wattle on their forehead, which dangles along their beak.

Extremely loud

The louder the screaming piha and white bellbird scream, the shorter their call will last, as investigation by Podos and Cohn-Haft showed. Apparently, it is demanding to make such a loud noise. So, females can deduce what a male’s quality is from the volume it produces. Females aim to mate a high-quality male, because that will yield healthy, strong offspring. Moreover, sons of such father will also be able to scream loudly, and so be attractive.

To assess the males’ quality on base of their sound volume, females have to come close to them. For bellbird females, which approach a male up to a meter distance, that is no fun, the biologists think. The males have two versions of their song: they usually shout roughly at the level of the screaming piha. But they are able to call even more loudly, like a pneumatic drill, no less than three times as loud as a screaming piha. A bellbird male is able to produce this sound because of its sturdy muscular body.

Risk

When a female approaches a male closely, he will choose the extremely loud version. He sings the first tone in a crouched position, head and tail bent downwards, his back towards her. Then he swivels around in a split second to blast the second, loudest tone right in her face.

She anticipates,  and flutters away when he is about to erupt, but still she is so close that she might suffer hearing damage.

Despite that risk, a female will still join different males, in order to be able to make a choice. It is in his interest to shout as loudly as possible to present himself favourably; it is in her interest to expose herself to that deafening noise, so that she is able to assess his quality.

Willy van Strien

Photo: White bellbird, singing male. ©Anselmo d’Affonseca

Watch and listen to a screaming white bellbird

Compare the sound of screaming piha and white bellbird

Source:
Podos, J. & M. Cohn-Haft, 2019. Extremely loud mating songs at close range in white bellbirds. Current Biology 29: R1055–R1069. Doi: 10.1016/j.cub.2019.09.028

Stripe suit or mohawk

Jumping spider males have two ways to approach cannibalistic females

Striped male Maevia inclemens reduces female aggression

The jumping spider Maevia inclemens is peculiar by having two types of males. They look different and they behave differently. Why would that be? The morphs have developed alternative strategies to reproduce safely, Laurel Lietzenmayer and colleagues think.

Tufted male Maevia inclemens signals its qualityIn the North American jumping spider Maevia inclemens, two types of males exist that differ so much, that they seem to be different species. Some males are black with pale legs and have three tufts of setae on their head, a bit like a cross-positioned mohawk. Other males have black-and-white striped legs and orange pedipalps (the ‘boxing gloves’).

So, females have the opportunity to choose between a punker and a male in a stripe suit. But the ladies are not choosy at all: they respond to the first male they happen to see.

The difference in appearance is linked to a different courtship behaviour. According to Laurel Lietzenmayer and colleagues, alternative strategies to reproduce are behind the differences, each male type being successful in its own way.

Signaling quality

The males face a difficult problem. To be able to reproduce, they must attract the attention of a female. But Maevia inclemens is a predatory species, and males are potential prey for females. Therefore, a male must manage to elicit a female’s mating behaviour – and not her appetite.

The tufted male will stay at a safe distance if he aims to mate a female, about 9 centimetres; the males are only half an inch in length, females are slightly larger. He makes himself as tall as possible by standing on three leg pairs and lifting himself tall, raising and clapping his front legs rhythmically; he also moves his pedipalps and abdomen.

The larger a male is, the higher his quality, the researchers assume. A female will probably prefer to copulate with a large male, because his offspring will inherit his superior qualities. The mohawk may give the female an extra clue about his size, because, as measurements show, the larger the male, the longer his tufts.

Avoiding cannibalism

A striped male has to come closer to a female to attract her attention, because she is not able to discern him easily at a great distance. He courts at only 3 centimetres from her, running the risk of being cannibalized. He makes himself as small as possible by crouching and he slides in semicircles, while holding his front legs in a triangle-like configuration.

Experiments with prey (termites) in different capes of coloured paper show that potential prey with a black-and-white stripe pattern is more conspicuous. Still, it is not attacked more frequently than prey with a solid gray or orange colour. Apparently, the stripes suppress the aggression of female Maevia inclemens, perhaps because many striped prey species are venomous.

Two solutions

Both types of males seem to have a different solution for the problem of approaching a cannibalistic female, the researchers write, which is reflected in their dimorphic appearance and behaviour. The tufted male signals his quality at a far distance, while the striped male attracts her attention while reducing her aggression from nearby. In other words: the tufted male tries to stimulate her mating behaviour, the striped male to temper her appetite.

If a female is willing, the encounter follows the same pattern for both male types. They behave the same, have the same chance of mating successfully and on average sire the same number of offspring. After mating, they again run the risk of being consumed, but in almost all instances they are able to escape.

Genetic determined?

The story about the alternative strategies of Maevia inclemens males is not yet complete, Lietzenmayer indicates. Many questions are still open, for example: is a female actually able to estimate the size of a tufted male from his tufts’ length? Are courting males with striped legs really more visible from close distance than solid coloured males?

In addition, it is not yet known whether the difference between the male types is genetically determined and how it originated.

Few animal species are known with different male types. This remarkable jumping spider is one of them, and it will be fascinating to find out why.

Willy van Strien

Photos:
Large: Maevia inclemens, striped male. Opoterser (Wikimedia Commons, Creative Commons CC BY 3.0)
Small: Maevia inclemens, tufted male. Tibor Nagy (via Flickr, CC BY-NC-ND 2.0)

Watch both male types courting

Sources:
Lietzenmayer, L.B., D.L. Clark & L.A. Taylor, 2019. The role of male coloration and ornamentation in potential alternative mating strategies of the dimorphic jumping spider, Maevia inclemens. Behavioral Ecology and Sociobiology 73: 83. Doi: 10.1007/s00265-019-2691-y
Clark, D.L. & B. Biesiadecki, 2002. Mating success and alternative reproductive strategies of the dimorphic jumping spider, Maevia inclemens (Araneae, Salticidae). The Journal of Arachnology 30: 511-518. Doi: 10.1636/0161-8202(2002)030[0511:MSAARS]2.0.CO;2
Clark, D.L., 1994. Sequence analysis of courtship behavior in the dimorphic jumping spider Maevia inclemens (Araneae, Salticidae). The Journal of Arachnology 22 : 94-107.

Pair bonds in bats

Female Egyptian fruit bat selects male that shared its food

In Egyptian fruit bat, a fruit-eating mammal, males take the initiative to mate, but females determine whether mating occurs. They strongly prefer a friend that often offered them food, Lee Harten and colleagues write.

Bats are social animals, and so is the Egyptian fruit bat (Rousettus aegyptiacus), which occurs in Africa and the Middle East. The fruit-eating mammals live in large colonies of up to thousands of specimens. Individuals within a group maintain friendship bonds with a few others, meaning that they share food.

Lee Harten and colleagues previously reported that the animals have two ways to obtain food. A risky way is to get fruit from a tree on their own. When a bat lands in a tree to collect food, it runs the risk of being caught by a predator, such as a snake or a cat. Therefore, the bats forage high in the trees. And when a fruit tree has thin foliage, they fly with their catch to a safe place to consume it.

There is also a funky method that the bats often use. If a colony mate holds a fruit in its mouth, they approach it and try to steal it. The bat that has obtained the fruit may respond aggressively, but sometimes it will have its catch scrounged.

Faint-hearted

Individuals differ in their strategy. Some usually pick their own fruit, while others are more likely to try to scrounge it. The scroungers are more anxious. They are afraid to land on a place with food, and if they do, they are so vigilant that most times, they will not be able to pick any fruit. For faint-hearted bats, scrounging from others is the better option.

Often scroungers don’t approach any arbitrary colony member, but they have one or two partners that they regularly approach, and that tolerate it. So, a network of affiliations exists.

Overall, Egyptian fruit bat males and females use different strategies. Males are more likely to collect fruit on their own than to scrounge, while for females it is the other way around. Only during lactation – a female produces one pup once or twice a year – they shift to collecting food on their own; they then need extra energy. Outside that period, they prefer to scrounge, each from its own set of favorite males.

Reciprocity

Now, Harten shows that those relationships have big consequences. In his lab, he kept a colony of wild-born Egyptian fruit bats, fifteen males, ten females and the young that were born in the lab. Genetic paternity analysis of the pups showed that in most cases, the father was one of the males that the mother preferred to get food from. The transfer of food from father to mother had been most intensive in the period just before pregnancy.

It is not a direct exchange of food for sex, because not all food-sharing bonds result in a descendant. But by tolerating a few females to prig food, a male has a chance to sire offspring later. Although a male takes the initiative to mate, a female decides whether or not to accept it. If she does, the male gets something in return for its generosity. Such delayed reciprocity is probably an explanation, but maybe not the only one, that the animals share food with some others.

Each male has a number of regular scroungers and a chance to produce a young with one of them. The relationships persist during a breeding season, but when a new period starts, females select another male to sire their young.

Willy van Strien

Photo: Egyptian fruit bat with fig. Artemy Voikhansky (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Sources:
Harten, L., Y. Prat, S.B. Cohen, R. Dor & Y. Yovel, 2019. Food for sex in bats revealed as producer males reproduce with scrounging females. Current Biology, online May 23. Doi: 10.1016/j.cub.2019.04.066
Harten, L., Y. Matalon, N. Galli, H. Navon, R. Dor & Y. Yovel, 2018. Persistent producer-scrounger relationships in bats. Science Advances 4: e1603293. Doi: 10.1126/sciadv.1603293

Discrete invitation

Arabian babbler leads partner to hidden place

Arabian babbler invites partner in an unobtrusive way

Unlike other animals, the Arabian babbler keeps its sex life private. It has a subtle way to invite another bird for a concealed copulation, as Yitzchak Ben Mocha and colleagues observed.

Animals do not seek to conceal their sexual behaviour. But the Arabian babbler, Argya squamiceps, is an exception. The birds, which live in stable kin groups of two to twenty individuals, do not want to be detected when copulating. A couple that is going to mate will take care to be out of sight of their group mates: at a certain distance or behind thick vegetation.

Yitzchak Ben Mocha and colleagues describe how the birds take a partner to such hidden place without revealing their intention to the other birds.

Arabian babblers live in open, dry landscapes across the Arabian Peninsula and Israel, where each group defends a territory. Within a group, only one pair, the dominant pair, will breed. They are the parents of nearly all young in the group. The other adult group members are subordinates and help raise the young. After hatching, the young stay in the nest for two weeks. And after fledging, it takes another eight weeks until they reach independency. During this period, they need care: protection and food.

Unobtrusive

Observing a population, the researchers witnessed that the birds have a subtle way to invite another bird to copulate. They place themselves in a location that is visible to that specific bird only while holding an object in the beak; often they slightly shake their head. The object can be anything, such as a twig, leaf, fruit, small animal or eggshell. The signalling behaviour is unobtrusive, but the partner grasps the message. When he or she accepts the invitation and approaches, the initiator moves away or hides behind the vegetation and the partner will follow. If they lose contact, the initiator comes back, places itself within the other’s visual field and repeats the invitation.

Usually, a copulation follows. But when another group member appears, the  signaller drops the object and stops the mating behaviour.

The object presented is nothing special, just something that happens to be abundant. So, it is not intended to impress. Neither is it a gift; although it may be edible, that does not affect the partner’s response. The presentation is just a subtle way to invite a mate for a concealed copulation.

Crucial help

Even dominant birds, which don’t have to fear that subordinates will dare to disturb a copulation, take great care to hide their mating behaviour. Why is that? The authors offer an explanation. The care of subordinate group members is crucial for raising the offspring. Without that care, the young have a smaller chance to reach adulthood. Moreover, they gain less weight and will be less capable to acquire food once they are independent.

The dominant pair does not want to lose that precious help. With overt mating behaviour, the researchers suggest, they would cause social tension in the group and increase the chance that subordinates leave or fight, which would be undesirable. So, the parents prefer to keep peace by keeping their love life private.

Willy van Strien

Photo: Greg Schechter (Wikimedia Commons, Creative Commons CC BY 2.0)

See invitation for concealed copulation on YouTube

Sources:
Ben Mocha, Y. & S. Pika, 2019. Intentional presentation of objects in cooperatively breeding Arabian babblers (Turdoides squamiceps). Frontiers in Ecology and Evolution 7: 87. Doi: 10.3389/fevo.2019.00087
Ben Mocha, Y., R. Mundry & S. Pika, 2018. Why hide? Concealed sex in dominant Arabian babblers (Turdoides squamiceps) in the wild. Evolution and Human Behavior 39: 575-582. Doi: 10.1016/j.evolhumbehav.2018.05.009
Ridley, A.R., 2007. Factors affecting offspring survival and development in a cooperative bird: social, maternal and environmental effects. Journal of AnimalEcology 76: 750-760. Doi: 10.1111/j.1365-2656.2007.01248.x

Costs before benefits

By guarding stepkids, bee male may get the mother

In bee Ceratina nigrolabiata, the male takes care of other males' offspring

Ceratina nigrolabiata bee males guard the nest of their female partner. This seems surprising, as the brood consists mainly of other males’ offspring, as Michael Mikás and colleagues show. Still, the males have good reason.

Bee males don’t do much. Okay, they mate with females and of course that is important, but that’s it. The females construct a nest and take care of the offspring. In solitary species, such as the species that visit a bee hotel, each female makes her own nest; social species, such as the honeybee, live in groups in which queens produce eggs and workers do the work.

There is one exception, Michael Mikát and colleagues report: in the solitary bee species Ceratina nigrolabiata, males do participate in care – but, surprisingly, mainly by protecting other males’ offspring.

Guard

A Ceratina nigrolabiata female makes her nest in the hollow stem of a plant. She goes inside, lays an egg, brings food for the larva that will hatch, closes the space by building a wall and lays another egg in the next part of the stem. Ultimately, a nest consists of six to seven cells in a row, with young in a descending stage of development when viewed from the inside out. The mother leaves when the nest is completely provisioned.

In the majority of nests in which a female is active, a male is present, as the researchers observed during their studies in the Czech Republic. When the female performs foraging trips, the male stays inside the nest to protect it from predators such as ants, driving them away when they come near. He is sitting near the entrance with the head facing inwards. When she returns, she will scratch his abdomen and he will let her pass.

The benefit for her is clear: thanks to this guard, she can leave to forage without having her nest unattended.

For him, it is different. DNA analyzes show that in most cases the brood that he protects does not contain any offspring that he fathers. So he takes care of other males’ offspring, and in general, that is not a good strategy from an evolutionary point of view.

Male switches

In fact, the bee males have no interest in the brood at all; it is the mother that captivates them. A male only has a chance to mate if he finds a female and stays with her until she is willing; in Ceratina nigrolabiata, a female will mate several times in her life. So he has to stay at her nest. While he certainly participates in care by actively protecting the brood, this stepfather care is a by-product of monopolizing a female, according to the researchers.

And indeed, if they removed a female from her nest, the male abandoned the brood.

So, every female is assured of a helpful lover. If a male disappears, his place is usually taken by another.

These stepfathers are not ideal helpers, because they stay on average for only seven days, while a female needs about forty days to complete her nest. As a consequence, the male inhabitant of most nests changes one or more times, and in fatherless periods the female spends less time collecting food, staying on the nest instead. The more changes, the fewer offspring she therefore can produce. But at least she gets help, which is unique among solitary bees.

Willy van Strien

Photo: Ceratina nigrolabiata, female returns at her nest in a hollow plant stem and scratches the guarding male. ©Lukáš Janošík

Source:
Mikát, M., L. Janošík, K. Cerná, E. Matoušková, J. Hadrava, V. Bureš & J. Straka, 2019. Polyandrous bee provides extended offspring care biparentally as an alternative to monandry based eusociality. PNAS: 116: 6238-6243. Doi: 10.1073/pnas.1810092116

Humboldt squid doesn’t discriminate

Sperm to both male and female partners

Humboldt squid male mates male and female partners

Males of the humboldt squid are generous with their sperm cells; male-to-male mating is as common as male-to-female mating, Henk-Jan Hoving and colleagues discovered.

The mating of the humboldt squid or jumbo squid, Dosidicus gigas, is peculiar. Males produce spermatophores, long narrow capsules in which sperm cells are packed, and deposit them around a partner’s beak, which is between the eight arms and two tentacles. Each spermatophore then turns itself inside out to form a so-called spermatangium, which attaches itself to the skin.

If the partner is a female, the sperm cells will be needed. When she is spawning, she will use the sperm cells to fertilize the eggs. But the males transfer their sperm packets not only to females, but also to other males, according to Henk-Jan Hoving and colleagues. And males can’t use them.

It is not possible for researchers to directly observe the mating behaviour of the squid, which occurs in the eastern Pacific Ocean, because the animals live at a depth of several hundred meters. Instead, in order to learn something about that behaviour, the team examined the buccal area of captive specimens, both males and females, and counted the implanted spermatangia. They found sperm packets attached to both females’ and males’ buccal tissues, the same number in both sexes. The motto of mating males seems to be: ‘deposit your spermatophores anywhere you can’.

The question is why they don’t distinguish between male and female partners, as sperm cells transferred to a male are wasted.

Sharp teeth

The authors offer an explanation. The animals live in large mixed schools, in which they encounter many females and males. External morphological differences between the sexes are small, and a male that is about to mate has little time to check whether the individual in front of him is female. If he doesn’t manage to deliver his spermatophores quickly between the other squid’s arms and tentacles, he is in danger to be attacked. The humboldt squid is a predator; the suckers on its tentacles are lined with sharp teeth and its mouth has sharp edges. Cannibalism occurs.

That is why a male prefers a partner that is not larger, but of similar size. Because males are on average smaller than females, he will often deposit his spermatophores on a female that is not yet sexually mature. That is okay; she will store it until she needs it. But there is a chance that he accidentally transfers his sperm to a male.

Because of this strategy – be fast and stay safe – a humboldt squid male admittedly will waste sperm. But that is not a serious drawback. A male has hundreds of spermatophores available, and no more than 80 are transferred per mating. Even if he often mistakenly chooses a same-sex partner, he can still mate many females.

Storage

A female has dozens of sperm-storage organs in the buccal membrane, the seminal receptacles. Sperm cells leave the spermatangium after mating and migrate over the female skin to those storage organs, which apparently secrete an attractant.

When spawning, a female releases millions of eggs, held together in a gelatinous spherical mass. When that mass of eggs passes her mouth, the sperm cells will leave the storage organs, swim to the egg mass and fertilize the eggs.

Willy van Strien

Photo: Foto: Humboldt squid. Rick Starr. Credit: NOAA/CBNMS (Wikimedia Commons, Creative Commons CC BY 2.0)

Sources:
Hoving, H-J.T. Fernández‑Álvarez, F.Á., E.J. Portner & W.F. Gilly, 2019. Same‑sex sexual behaviour in an oceanic ommastrephid squid, Dosidicus gigas (Humboldt squid). Marine Biology 166: 33. Doi: 10.1007/s00227-019-3476-6
Fernández-Álvarez, F.Á., R. Villanueva, H-J.T. Hoving & W.F. Gilly, 2018. The journey of squid sperm. Reviews in Fish Biology and Fisheries 28: 191-199. Doi: 10.1007/s11160-017-9498-6

Romantic sea

Fairytale light shows of Cypridinid ostracods

ostracod produces light to escape from predator

With an amazing show of light pulses, male cypridinid ostracods try to attract a mate. Each species has its own specific show program, with either very short lasting flashes or bulbs that glow for several seconds. Nicholai Hensley and colleagues examined the chemistry behind.

It looks like a fairytale scene: dozens of blue lights dancing in the dark waters of the Caribbean Sea. The spectacle is visible to those who dive or snorkel at the beginning of the night. The light artists are ostracods of the Cypridinidae family, tiny crustaceans (less than two millimeters long) with a carapax consisting of two valves, like a clam shell.

They are also known as sea fireflies. Nicholai Hensley and colleagues study their behaviour and the chemistry behind their light.

Slimeballs

Ostracods produce light by expelling mucus containing a reactant, vargulin, and the enzyme c-luciferase, which react with oxygen in seawater emitting blue light. The ostracods use their light mainly to avoid predation. If a fish picks up an ostracod, the prey will produce a cloud of blue mucus that is pumped into the water via the gills of the fish. It makes the fish visible to its own predators. Startled, it will spit out the bite.

In ostracods of the family Cypridinidae that live in the Caribbean Sea, males use the same light reaction in a much more subtle way with a completely different purpose: they place luminescent slimeballs in the water in order to seduce a female into a mating. This courtship behaviour produces the fairytale scenes.

Train of lights

The light artist best known is Photeros annecohenae, one of the most abundant species off the coast of Belize. In the first dark hour of the night, when the sun is down and the moon is not shining, groups of males display above seagrass beds. They have to perform well, because competition is high. While there are as many females as males, most are unavailable. This is because they incubate fertilized eggs in a brood pouch, and during this period, they will not mate.

American biologists examined male courtship behaviour in the lab, using infrared light. A displaying male will first swim in a looping pattern just above the tips of the seagrass blades and place about three bright flashes of light, probably to draw attention. Then, while spirally swimming upward, it places weaker light pulses at regular intervals. It swims at high speed, slowing down when it releases a luminescent slime ball.

By doing so, it creates a train of about twelve consecutively flashing lights that can be 60 centimetres long. When finished, it descends to start a new series. Often other males join and start displaying in synchrony.

Interception

To choose a mate, females assess the light pulses that the males produce. If a female is attracted to a particular male, she will swim to him without producing any light herself. Thanks to his regular flashing pattern, she manages to meet him just above his last light pulse. Mission accomplished.

Sometimes males try to obtain a mate without producing light themselves. Instead, they intercept a female that is on her way to a performing male.

Starting a show, following another male’s show or sneaking to get a female are different tactics to acquire a mate and a male can easily switch among them.

Species-specific shows

In the Caribbean Sea, many other species of Cypridinidae also occur, and about ten species commonly live at the same place. Because they all have their own characteristic light show, a female has no difficulty finding a conspecific partner. The shows vary in the trajectory a courting male swims, the number of light pulses, the brightness of the light, the interpulse distance and time interval and the time that a pulse remains visible.

Romantic

Hensley investigated the cause of the variation in light pulse length. For although all species perform the same chemical reaction to make light pulses, the duration of the pulses varies greatly: some species, such as Photeros annecohenae, show flashes that last only a fraction of a second, others make light bulbs that continue to glow for 15 seconds.

The structure of the enzyme c-luciferase appears to vary between species, resulting in the light reaction to proceed faster in one species than in another. This determines how soon the light extinguishes. In addition, the reaction rate depends on the amount of vargulin compared to the amount of enzyme: the more vargulin, the longer it takes before it is all converted and the light disappears.

Courting males produce far less light than an animal that avoids predation. Romantic lights don’t have to be that big and bright.

Willy van Strien

Photo: Luminous cloud around a fish that intended to consume an ostracod. It will spit it out. © Trevor Rivers & Nicholai Hensley

Fifteen-scaled worm emits light to defend itself in another way

Sources:
Hensley, N.M., E.A. Ellis, G.A. Gerrish, E. Torres, J.P. Frawley, T.H. Oakley & T.J. Rivers, 2019. Phenotypic evolution shaped by current enzyme function in the bioluminescent courtship signals of sea fireflies. Proceedings of the Royal Society B 286: 20182621. Doi: 10.1098/rspb.2018.2621
Rivers, T.J. & J.G. Morin, 2013. Female ostracods respond to and intercept artificial conspecific male luminescent courtship displays. Behavioral Ecology 24: 877–887. Doi: 10.1093/beheco/art022
Rivers, T.J. & J.G. Morin, 2012. The relative cost of using luminescence for sex and defense: light budgets in cypridinid ostracods. The Journal of Experimental Biology 215, 2860-2868. Doi: 10.1242/jeb.072017
Morin, J.G. & A.C. Cohen, 2010. It’s all about sex: bioluminescent courtship displays, morphological variation and sexual selection in two new genera of Caribbean ostracodes. Journal of Crustacean Biology 30: 56-67. Doi: 10.1651/09-3170.1
Rivers, T.J. & J.G. Morin, 2009. Plasticity of male mating behaviour in a marine bioluminescent ostracod in both time and space. Animal Behaviour 78: 723-734. Doi: 10.1016/j.anbehav.2009.06.020
Rivers, T.J. & J.G. Morin, 2008. Complex sexual courtship displays by luminescent male marine ostracods. The Journal of Experimental Biology 211: 2252-2262. Doi: 10.1242/jeb.011130

Giving everything he’s got

Hummingbird male shines for a split second

broad-tailed hummingbird male performs spectacular dive

In order to seduce as many females as possible, a broad-tailed hummingbird male performs tight diving courtship flights. He combines movement, colour and sound into a spectacular whole, Ben Hogan and Cassie Stoddard show.

With a striking display, a broad-tailed hummingbird male (Selasphorus platycercus) tries to gain a female’s interest. He performs a number of U-shaped dives, getting down from great height (up to 30 meters!) while his wings are trilling. The lowest point of the dive is close to the targeted female, which is perched. At that point, he will give everything he’s got: he rushes past her with a top speed of more than 20 meters per second while his tail feathers produce buzzing sounds. The female perceives his iridescent gorget rapidly shifting from bright red to dark green. Then he climbs up to enable a new dive.

The show is so fast that we can’t see what exactly happens. But Ben Hogan and Cassie Stoddard made video and audio recordings of a large number of shows and analyzed them.

Blink of an eye

An entire dive takes about 6.5 seconds. At the lowest point, the small bird appears to tightly synchronize the components of the show, as the analysis revealed. As a result, top speed, buzzing sounds and colour change almost coincide, all occurring within 300 milliseconds, a human blink of the eye. When he rapidly rises again from the lowest point, the pitch of wing- and tail-generated sounds drops sharply, as when a car with a siren is passing by (the Doppler effect).

The whole is meant to make an overwhelming impression on her. But she is used to see shows like his, because all males perform them. The hummingbird males do not contribute to nest construction or care for the young, leaving all of the work to the females. They try to sire young with as many females as possible. With their tightly synchronized dive, they advertise their genetic quality, promising healthy and attractive offspring.

But is he able to seduce a female? The researchers have not yet figured out what exactly makes a show appealing and how it is performed perfectly in her eyes.

Willy van Strien

Photo: Greg Schechter (Flickr/Wikimedia Commons, Creative Commons CC BY 2.0)

Source:
Hogan, B.G. & M.C. Stoddard, 2018. Synchronization of speed, sound and iridescent color in a hummingbird aerial courtship dive. Nature Communications 9: 5260. Doi: 10.1038/s41467-018-07562-7