From so simple a beginning

Evolution and Biodiversity

Page 7 of 19

Wandering dragonfly

Globe skimmer travels thousands of kilometres

globe skimmers travel large distances

The dragonfly Pantala flavescens, the globe skimmer, was already known to be a migrating species that travels enormous distances. By conducting chemical analyses of the wings, Keith Hobson and colleagues once again confirm this picture.

It is well known that some butterflies migrate between widely separated regions where they spend summer and winter: monarch butterfly and painted lady. It is less known that two species of dragonflies exist that don’t refrain from undertaking a long journey either: the spot-winged glider, Pantala hymenaea, from North, Central and South America, and above all the globe skimmer dragonfly Pantala flavescens, which has an almost worldwide distribution. These species belong to the family Libelludae.

globe skimmer resting during migrationEarlier research by Daniel Troast had shown that no genetic differences exist between globe skimmer populations from North America (US), South America (Guyana) and Asia (India, Korea and Japan). This means that these populations are in contact with each other. In other words: the insects must be able to travel great distances.

Unique achievement

And they do, according to chemical analyses of the wings by Keith Dobson and colleagues. These analyses focus on the ratio of hydrogen isotopes, which corresponds to that of the water in which the dragonflies lived during their larval stage. The hydrogen isotopic composition of water bodies depends on precipitation and temperature.

Earlier, Hobson had elucidated how globe skimmers migrate annually from Northern India, or perhaps even across the Himalayas, to East Africa and back. The total distance per cycle is at least 18,000 kilometres and it takes several generations to complete it. An individual dragonfly travels up to 6,000 kilometres during its lifetime, and many individuals fly 3,500 kilometres across the ocean. That is a unique achievement in the insect world.

During flight, migrating dragonflies catch small prey from the sky. They fly at high altitudes, probably using winds that are associated with the so-called Intertropical Convergence Zone. The zone changes position during the year, causing wind and unstable weather.

Summer migrants in Japan

Now, Hobson took a look at globe skimmers that occur in Japan in summer. They can be found from April to November and occur in large numbers from June to September. Most of Japan is too cold for them in winter, so they don’t hibernate there. When they appear in spring, they come from elsewhere, thousands of kilometres away.

As the wing analyses revealed, the first specimens, in April, probably come from the southwest: South China and Southeast Asia. Later, in the summer, dragonflies arrive from the west: North China and Mongolia, or from South China, North India and the Tibetan Plateau. Might the latter trip be a continuation of the journey that the animals take from East Africa? Unfortunately, the researchers don’t mention it.

Still later, in October and November, dragonflies keep coming from the west; Hobson also found insects from Korea and the east of Russia. Only a few animals had grown up in Japan. The migration appears to be related to the wind direction, which is predominantly westerly in summer.

Rapid development

The wandering existence of the globe skimmer is partly possible because the larvae develop rapidly. While that development takes ten months in other species, the globe skimmer needs about six weeks. And then migration can continue.

This short development time also means that globe skimmer dragonflies are not dependent on areas with permanent water bodies for reproduction. Females can also use temporary water bodies from rainy periods to lay eggs in.

Willy van Strien

Photos
Large: The globe skimmer dragonfly, Pantala flavescens. Rison Thumboor (Wikimedia Commons, Creative Commons CC BY 2.0)
Small: Resting globe skimmers. Shyamal (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Another migrating insect: painted lady

Sources:
Hobson, K.A., H. Jinguji, Y. Ichikawa, J.W. Kusack & R.C. Anderson, 2020. Long-distance migration of the globe skimmer dragonfly to Japan revealed using stable hydrogen (δ 2H) isotopes. Environmental Entomology, online Nov. 21. Doi: 10.1093/ee/nvaa147
Troast, D., F. Suhling, H. Jinguji, G. Sahlén & J. War, 2016. A global population genetic study of Pantala flavescens. PLoS ONE 11: e0148949. Doi: 10.1371/journal.pone.0148949
Hobson, K.A., R.C. Anderson, D.X. Soto & L.I. Wassenaar, 2012. Isotopic evidence that dragonflies (Pantala flavescens) migrating through the Maldives come from the northern Indian subcontinent. PLoS ONE 7: e52594. Doi: 10.1371/journal.pone.0052594

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

Acid gulp

Ant swallows its own formic acid to stay healthy

Tnaks to formic acid, Formicinae ants are healthy

Formic acid appears to be a great help for ants to prevent infection from contaminated food, Simon Tragust and colleagues discovered. A gulp after each consumption increases their survival chance.

People like sweet desserts, but for ants of the subfamily Formicinae it is different. They take a gulp of formic acid after eating or drinking, Simon Tragust and colleagues witnessed.

This is remarkable, because formic acid is an aggressive substance. Formicinae ants produce it in a venom gland that has an opening at the tip of the abdomen. They were known to spray it at predators, such as birds, spiders, and insects, to defend themselves, and this is understandable. But swallowing?

Disinfect

Tragust and colleagues had shown previously that Formicinae ants use their acid not only against predators, but also against pathogens. Workers apply it in combination with resin to keep an entomopathogenic fungus (Metarhizium brunneum) out of their nest.

Also, they use formic acid to keep the brood clean. If they detect pupae covered with spores of the pathogenic fungus, they clean them and cover them with formic acid, which they had taken up from the abdominal gland opening into the mouth.

If fungal spores have already germinated on a pupa and the fungus has penetrated the cuticle, workers unpack the infected pupa from its cocoon, bite holes in the skin and inject formic acid. In this way, they prevent the fungus from growing and forming spores that will contaminate the rest of the colony. The pupa does not survive the treatment, but it would have been killed by the fungus anyway.

Crop acidity

Now, a new application of formic acid comes to light: Formicinae ants swallow their own formic acid after eating or drinking something. Tragust deduces this from tests in the lab with Florida carpenter ant, Camponotus floridanus. He offered ants honey water or plain water and saw them lick their abdominal tip afterwards. Apparently, they then took up acid into the mouth and swallowed it, as Tragust showed that the contents of their crop, just before the stomach, became very acidic.

Perhaps, the idea was, workers take formic acid to kill bacteria that may be present on food. And that was the case, as became clear from tests in which workers were given food that was contaminated with a pathogenic bacterium species (Serratia marcescens). In ants that then took a gulp of formic acid, bacteria did not survive the crop environment and the rest of the intestinal system remained clean. Ants that were prevented from taking in acid, were at greater risk of a deadly infection.

Only bacteria that thrive in acidic environments survive the acidic crop, and such bacteria populate the ants’ intestines. But these are beneficial bacteria that help digest food. The acid appears to be an excellent remedy against pathogenic microbes.

Fortunately, we don’t have to take an extremely sour dessert like Formicinae ants, because our stomach keeps itself acidic.

Willy van Strien

Photo: Carpenter ant, Camponotus cf. nicobarensis. ©Simon Tragust

Ants also use formic acid to keep fungus out of nest

Sources:
Tragust, S., C. Herrmann, J. Häfner, R. Braasch, C. Tilgen, M. Hoock, M.A. Milidakis, R. Gross & H. Feldhaar, 2020. Formicine ants swallow their highly acidic poison for gut microbial selection and control. eLife 9: e60287. Doi: 10.7554/eLife.60287
Pull, C.D., L.V. Ugelvig, F. Wiesenhofer, A.V. Grasse, S. Tragust, T. Schmitt, M.J.F. Brown & S. Cremer, 2018. Destructive disinfection of infected brood prevents systemic disease spread in ant colonies. eLife 7: e32073. Doi: 10.7554/eLife.32073
Tragust, S., B. Mitteregger, V. Barone, M. Konrad, L.V. Ugelvig & S. Cremer, 2013. Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. Current Biology 23: 76-82. Doi: 10.1016/j.cub.2012.11.034

Is it an ant?

Jumping spider exchanges jumping proficiency for safety

Myrmarachne jumping spiders resemble ants

To escape from predators, some jumping spider species mimic the appearance of an ant. A smart move, but it may constrain jumping abilities, Yoshiaki Hashimoto and colleagues supposed.

Everyone can tell the difference between a spider and an ant. A spider’s body has two parts: a cephalothorax and an abdomen, which is usually round. It has eight legs. An ant, on the other hand, is slender. Head and thorax are separated, while the abdomen is connected to the thorax by a narrow pedicel. It has six legs and two antennae.

But you can be mistaken, because some jumping spiders, Myrmarachne species, convincingly mimic the appearance of a spider. This is at the expense of their jumping skills, Yoshiaki Hashimoto and colleagues show.

It will certainly be beneficial for these little spiders to look like an ant. Predators refrain from taking an ant, because this prey may bite or sting, spray formic acid or have an army of colleagues nearby. They also avoid spiders that look like an ant.

Complete picture

The jumping spiders imitate ants in several ways. Females of Myrmarachne plataleoides, for example, resemble the green weaver ant (Oecophylla smaragdina) very closely. They are the same size and colour. The shape is also similar, thanks to a constriction behind the head and an elongated pedicel between a slender thorax and a thin, long abdomen with an anterior constriction. Two black spots on the side of the head imitate the large eyes of ants; the eight real eyes at the front are hardly visible. And to complete the picture, these spiders often slightly lift the first pair of legs; it seems as if they have six legs and a two antennae, just like ants.

But Hashimoto wondered: are jumping spiders that mimic ants really jumping spiders? In other words, isn’t the disguise at the expense of their jumping abilities?

Jumping spiders don’t construct a web, but they hunt on the ground and jump to their prey. To jump, they stretch their legs. This not done with muscle power, but with power generated by liquid pressure: the spiders pump hemolymph, their variant of blood, from the abdomen into the cephalothorax, to which the legs are attached, and by compressing the cephalothorax, they raise the pressure, extending the legs. For ant mimics this is difficult, because they have to force the liquid through the thin stalk between the abdomen and the cephalothorax. And as the cephalothorax is thin, they cannot create high pressure. Hence the question.

Giant leap

The researchers took seven Myrmarachne species from tropical Southeast Asia and compared their shape with that of other jumping spider species. Myrmarachne-spiders were indeed more elongated and slenderer. Some ant mimics, including Myrmarachne plataleoides, were very slender because they mimic a very thin ant.

In a lab test, non-mimetic jumping spiders jumped a distance nearly three times their body length. The ant mimics didn’t perform as well. The very slender types only jumped two-thirds of their body length, the thicker ones went a bit further. So, ant-mimicking jumping spiders have indeed sacrificed their jumping ability in exchange for safety. That makes hunting more difficult, because they cannot jump on prey from a distance. Tests show that their prey capture success rate is lower than that of other jumping spiders.

There is some evidence, the researchers write, that the most slender ant mimics switched to a mainly plant-based diet. That would be a giant leap – albeit figuratively.

Willy van Strien

Photo: Jumping spider Myrmarachne plataleoides, female. Renjusplace (Wikimedia Commons, Creative Commons CC BY-SA 4.0)

Source:
Hashimoto, Y., T. Endo, T.Yamasaki, F.Hyodo & T. Itioka, 2020. Constraints on the jumping and prey‑capture abilities of ant‑mimicking spiders (Salticidae, Salticinae, Myrmarachne). Scientific Reports 10: 18279. Doi: 10.1038/s41598-020-75010-y

Successful clutch? Leave!

Plovers abandon successful family to re-nest elsewhere

Plovers, including snowy plover, leave their family when successful

A successful marriage triggers divorce, at least in plovers. That is because a parent that deserts may achieve higher reproductive success, Naerhulan Halimubieke and colleagues noted.

A bird male and female that successfully raised young had better stick together, you might think, as they have proven to be a good team. And after a disappointing breeding result, it is best for them to split up and find another mate, with which things may go better. Such is the behaviour in most species of birds in which pairs form to breed.

But in plovers, it is the other way round, Naerhulan Halimubieke and colleagues write. A pair of plover parents often will divorce after successfully producing chicks. And after nest failure, male and female stay together to try again. For these birds, this is the best strategy.

New brood

The researchers had previously found this pattern – divorce if successful, stick together if failing – in the snowy plover Charadrius nivosus, a ground-nesting bird which lives on sandy beaches. A clutch consists of three eggs in a shallow scrape, which are incubated by both parents. When the chicks hatch, they leave the nest immediately. They find their own food and only need warmth and protection from their parents. A single parent can easily provide this. It is therefore not necessary for both parents to stay with the young until they are completely independent, after about a month.

That is why one of the parents may leave its successful family to find a new mate and initiate another brood. Deserting parents gain time, taking advantage of the breeding season as much as possible; their behaviour results in more offspring on average within a breeding season.

Females desert more often than males, probably because there is a small surplus of adult males, so that on average, females meet a new mate sooner.

A completely different situation arises when a snowy plover brood fails, which in most cases is caused by a predator that detected the nest. The best strategy for the parents in that case is to stay together and start a new nest immediately.

Other plovers

Now, this appears to apply to other species of plovers as well, all of them shorebirds. Halimubieke and colleagues examined eight species. Populations with greater breeding success exhibit a higher rate of divorce within a breeding season than populations with less success, they noted. And within populations, couples with a successful clutch split up more often than couples that see their clutch fail.

Also over years, these birds are not necessarily faithful to their mates. When a new breeding season is coming, they start to nest as soon as possible without worrying too much about mate selection. Having as much offspring as possible – that’s the most important thing.

Willy van Strien

Photo: snowy plover, Charadrius nivosus. Lisa Mcgloin (Wikimedia Commons, Creative Commons CC BY 3.0)

Sources:
Halimubieke, N., K. Kupán, J.O. Valdebenito, V. Kubelka, M.C. Carmona‑Isunza, D. Burgas, D. Catlin, J.J.H. St Clair, J. Cohen, J. Figuerola, M. Yasué, M. Johnson, M. Mencarelli, M. Cruz‑López, M. Stantial, M.A. Weston, P. Lloyd, P. Que, T. Montalvo, U. Bansal, G.C. McDonald, Y. Liu, A. Kosztolányi & T. Székely, 2020. Successful breeding predicts divorce in plovers. Scientific Reports 10: 15576. Doi: 10.1038/s41598-020-72521-6
Halimubieke, N., J.O. Valdebenito, P. Harding, M. Cruz‐López, M.A. Serrano‐Meneses, R. James, K. Kupán & T. Székely, 2019. Mate fidelity in a polygamous shorebird, the snowy plover (Charadrius nivosus). Ecology and Evolution. 9: 10734-10745. Doi: 10.1002/ece3.5591

Well-timed flowering

Dodder eavesdrops on host plant’s signal

dodder manages to flower simultaneously with its host

Dodder, a plant that parasitizes other plants, flowers almost simultaneously with its host. The parasite takes up the host’s signal that activates flower development, Guojing Shen and colleagues show.

A plant may be covered with a tangle of thin, sticking threads. That is a bad condition for the plant, because those threads are stems of a parasitic plant: dodder (Cuscuta), of which about two hundred species exist worldwide. Most of them thrive on several host plant species. And whether a host flowers sooner or later in the season, dodder joins in and develops its flowers simultaneously. Guojing Shen and colleagues discovered how Australian dodder (Cuscuta australis) manages to synchronize its flowering time with that of its various hosts.

Once young dodder plants get hold of a host plant after germination, their roots disappear, so they cannot take up water and nutrients from the soil anymore. Also, they don’t have green leaves that take carbon dioxide from the air and convert it into carbohydrates with the help of sunlight, like other plants. Everything they need, they extract from the host, round the stems of which they wind extensively.

Maximum benefit

To exploit its host, the parasite forms numerous haustoria that penetrate into the host’s stems and connect with phloem, the tissue that transports organic compounds, and xylem, the tissue that transports water. The haustoria enable the parasite to extract nutrients and water from its victim.

Annual dodder species, like Cuscuta australis, first grow, then flower and eventually die. The parasite benefits most from its host when it flowers simultaneously. Because if it blooms earlier, it will not reach the size it could have reached by growing longer, and as a consequence it will produce fewer flowers and fewer seeds than it could have produced. But if it postpones flower development for too long, it will be short of nutrients during flowering. Because the host then channels as much nutrients as possible to its own flowers and seeds, leaving less to circulate in phloem and xylem from which dodder taps.

So, dodder has to adjust its flowering time to that of its host.

Dodder is eavesdropping

Most plants regulate their flowering time by tracking changes in day length. When it is about time for flowers to appear, the leaves produce the protein FT (flowering locus T), which moves through the phloem. This protein switches on flower development; it is, in other words, a mobile flowering signal.

Dodder would not benefit from having a flowering signal of its own. As it has to synchronize with its host, it must be flexible. It is therefore not surprising that it does not appear to have functional FT protein. There is a dodder variant of the protein, but it does not activate flowering. How then does the parasite regulate its flowering time?

By eavesdropping on the host’s flowering signal, Shen writes. He investigated flowering in Australian dodder, but the story will apply to other dodder species as well. To European dodder (Cuscuta europaea), for example, which can be found in Western Europe growing on nettle and hops; or to lesser dodder (Cuscuta epithymum), or hellweed, that grows on heather, broom, gorse, thyme and other plants.

It was already known that the parasite not only extracts water and nutrients from the host plant via haustoria, but that also several biologically active substances are exchanged.

Including the FT protein.

Perfect mechanism

As the host starts flower development and the plant produces FT protein, this is transferred to dodder. The researchers show that the host’s protein retains it activity in the parasite, initiating flower development there too.

And so the flowering time of the parasite will coincide nicely with that of its host. Eavesdropping is a perfect method for alignment.

Willy van Strien

Photo: Australian dodder, Cuscuta australis. Harry Rose (Wikimedia Commons, Creative Commons CC BY 2.0)

Watch the growth of fiveangled dodder (Cuscuta pentagona, from North America) on video

Sources:
Shen, G., N. Liu, J. Zhang, Y. Xu, I.T. Baldwin & J. Wu, 2020. Cuscuta australis (dodder) parasite eavesdrops on the host plants’ FT signals to flower. Proceedings of the National Academy of Sciences, online August 31. Doi: 10.1073/pnas.2009445117
Liu, N., G. Shen, Y. Xu, H. Liu, J. Zhang, S. Li, J. Li, C. Zhang, J. Qi, L. Wang & J. Wu, 2020. Extensive inter-plant protein transfer between Cuscuta parasites and their host plants. Molecular Plant 13, 573-585. Doi: 10.1016/j.molp.2019.12.002

True pregnancy

During gestation, pot-bellied seahorse males provision the embryos

Pregnant pot-bellied seahorse males provision the embryos

Seahorses are viviparous, and it is the males that are pregnant. In pot-bellied seahorse, Hippocampus abdominalis, males even provide the embryos with nutrients, Zoe Skalkos and colleagues discovered.

Some fish species are viviparous. In most cases, young fish are born from the mother, but in seahorses the father plays a unique role. He incubates the fertilized eggs in a fleshy, enclosed brood pouch until the offspring can live independently. In daddy’s pouch, the embryos are safe from small predators and pathogens. The pregnant father controls the water quality in the pouch; the highly vascularised pouch skin supplies oxygen and waste products are removed.

Males of pot-bellied or big-belly seahorse, Hippocampus abdominalis, that lives around Australia and New Zealand, also transport nutrients to their embryos, Zoe Skalkos and colleagues report.

Complex brood pouch

When seahorses mate, the female transfers her eggs into her partner’s brood pouch, which he has inflated by filling it with seawater. He fertilizes the eggs immediately and carries them until the young fish can be released. The developing embryos consume the large amount of high protein yolk that the eggs contain.

Pot-bellied seahorse is a large species, up to 35 centimeters long, and exhibits the most complex form of male pregnancy among seahorses. Young embryos are deeply embedded into the pouch’s lining tissue; some are completely covered. The embryos can survive on the amount of food that the yolk contains, according to experiments in which they developed outside a brood pouch. But young fish that are raised in this way exhibit stunted growth and suffer increased mortality. That is why the researchers wondered whether the pregnant father transports nutrients to his hundreds of young via the pouch wall.

Supplement

To find out, they compared the dry weight of newly fertilized eggs of pot-bellied seahorse with that of newborns, which are released after a gestation period of about 24 days. They also determined the fat content of eggs and newborns. From previous research, they knew that cell constituents that transport fats are produced in large quantities in the brood pouch of males during gestation. Fat is the primary source of energy for the embryos and they need a lot of it.

If the father would not supply nutrients to the embryos, the dry weight of newborn fish would be lower than that of newly fertilized eggs. That is because embryos consume the food supply that the mother provided; they gain weight, but part of the mass is lost by metabolism. The weight loss is estimated to be 30 to 40 percent.

However, as it turned out, newborns have the same dry weight as newly fertilized eggs. Also fat contents were similar. Most likely then, the father provides nutrition to his offspring, especially fats, to replace what is lost.

Pregnant in every sense

Pipefish are closely related to seahorses. Also in pipefish, fathers carry the embryos, although not all pipefish species possess a highly developed, enclosed brood pouch. In some pipefish species, as was known, pregnant males transport a small amount of nutrients to the embryos. Now, this also appears to happen in at least one seahorse species.

These fish dads are going through a pregnancy in every sense. However, compared to that of mammals, their pregnancy is not entirely complete, because the fish mothers still provide most nutrients to the embryos. But it certainly is extraordinary.

Willy van Strien

Photo: Pot-bellied seahorse mating. Elizabeth Haslam (Wikimedia Commons, Creative Commons CC BY 2.0)

Watch a video on courtship and birth in pot-bellied seahorse

Sources:
Skalkos, Z.M.G., J.U. Van Dyke & C.M. Whittington, 2020. Paternal nutrient provisioning during male pregnancy in the seahorse Hippocampus abdominalis. Journal of Comparative Physiology B 190: 547-556. Doi: 10.1007/s00360-020-01289-y
Whittington, C.M., O.W. Griffith, W. Qi, M.B. Thompson & A.B. Wilson, 2015. Seahorse brood pouch transcriptome reveals common genes associated with vertebrate pregnancy. Molecular Biology and Evolution 32: 3114-3131. Doi: 10.1093/molbev/msv177

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

Resemblance is striking

Parasitic Vidua nestlings trick host parents with near-perfect mimicry

Vidua nestlings mimic the young of their host parents

In order not to stand out in the nest in which they grow up clandestinely, Vidua nestlings mimic the young of the host parents. They perform very well, Gabriel Jamie and colleagues report. But some slight discrepancies exist.

African whydahs and indigobirds, Vidua species, are brood parasites like the cuckoo. They lay their eggs in the nest of other bird species, in this case grassfinches, and have the host parents raise their young. Vidua finches are unable to provide parental care. But these brood parasites do much less harm to the host families than a cuckoo, because young Viduas don’t eject other nestlings from the nest. The host parents take care for their own offspring, but have some extra, foreign young.

The foreign nestlings should not stand out, otherwise the tricked parents will notice the deception. It was already known that Vidua young resemble their host parents’ young. With special computer software, Gabriel Jamie and colleagues now show how successful the mimicry is.

Ornamented mouths

pin-tailed whydah is brood parasiteThe Vidua genus contains nineteen species. In the breeding period, the males are real beauties, while the females are inconspicuous and difficult to recognize. Jamie took a closer look at three species: pin-tailed whydah (Vidua macroura), broad-tailed paradise whydah (Vidua obtusa) and purple indigobird (Vidua purpurascens). They are host-specific, each Vidua species has a single host species. Jamie compared the Vidua nestlings to that of their respective host parents and of a number of other grassfinch species.

Young grassfinches (Estrildidae) have ornamental mouth markings that become fully visible when they open their beaks; this ornamentation in unusual among birds. Each grassfinch species has its characteristic pattern, colour and structure.

Nestlings of the breeding parasites accurately mimic those characteristic markings, is the conclusion of the research. An analysis with pattern recognition software shows that the pattern is similar to that of their host parent species. The colours match well too. Vidua nestlings also cleverly imitate the begging calls and postures of their foster siblings.

Imprinting

Previous research, by Michael Sorenson, had shown that the nineteen species of whydahs and indigobirds are much younger than their hosts in an evolutionary sense. The idea is that their common ancestor switched to a brood parasitic lifestyle with a grassfinch as host parent.

Speciation could then occur quickly. Whenever a Vidua female happens to lay eggs in the nest of another host, a separate group associated to that new host arises, because Vidua nestlings imprint on the song of their host father. Each grassfinch species has its own characteristic song. When grown up, Vidua males will mimic the song of their host, and females are attracted to this song. Also, females select a nest of the host species they were raised by to lay their eggs in. The group turns into a new species.

The nestlings then become more and more similar to the nestlings of the new host through an evolutionary adaptation process. Because the more a Vidua nestling resembles the young of its host parents, the more likely they are to accept it and care for it, increasing its survival chance.

Exaggerated

And as a matter of fact, the resemblance between foreign and own young in a parasitized grassfinch’s nest turned out to be striking. But it is not entirely perfect. Small but consistent differences exist. Perhaps the foreign nestlings are (yet) unable to fully mimic their nest mates. And apparently, they are doing well enough: the host parents accept them.

But there may be another explanation for the discrepancies, the researchers write. Nestlings of pin-tailed whydah, for example, have spots in the beak that are slightly larger than those of their foster parents’ young, common waxbill (Estrilda astrild), and their begging calls are slightly extended. Unlike a waxbill nestling, they wave a wing under their open mouth while begging.

So, these Vidua nestlings are slightly exaggerating their host’s begging signals. And perhaps the host parents favour them as a consequence. An intriguing thought.

Willy van Strien

Photos:
Large: pin-tailed whydah nestling, the outside of the mouth markings visible. ©Gabriel A. Jamie
Small: pin-tailed whydah, breeding male. Alan Manson (Wikimedia Commons, Creative Commons CC BY-SA 2.0)

Sources:
Jamie, G.A., S.M. Van Belleghem, B.G. Hogan, S. Hamama, C. Moya, J. Troscianko, M.C. Stoddard, R.M. Kilner & C.N. Spottiswoode, 2020. Multimodal mimicry of hosts in a radiation of parasitic finches. Evolution, online July 21. Doi: 10.1111/evo.14057
Sorenson, M.D., K.M. Sefc & R.B. Payne, 2003. Speciation by host switch in brood parasitic indigobirds. Nature 424: 928-931. Doi: 10.1038/nature01863

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

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