Banded Mongoose: mutualism, cooperative breeding, and vital adaptations

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 Banded mongooses in Kruger National Park, South Africa (Peet van Schalkwyk ©)

“It is the hardest thing in the world to frighten a mongoose, because he is eaten up from nose to tail with curiosity. The motto of all the mongoose family is ‘Run and find out'” —Rudyard Kipling, Rikki-Tikki-Tavi

Cultural inheritance in banded mongooses

The banded mongoose is a bit of an anomaly in the mammal world. Instead of the offspring being raised by their parents (and behaving similarly to their parents), they instead inherit their behaviors from other adult mongooses. The adults are random, rather than closely related to the offspring, but take on a parental role in the sense that they sort of “adopt” a baby/juvenile (about one month old) and show it how to forage, hunt, stay safe from predators, and otherwise be a mongoose properly. These role models or “escorts” will carry around the pups and teach them closely for about two months. The plasticity of mongoose behavior is sufficient to allow for pups to behave more similarly to their role models than to their parents.

This kind of transmittance of behavior is known as cultural inheritance, and is actually quite common in the animal world– but the unique setup in mongooses provides an opportunity to easily decouple the direct genetic inheritance from parents and the cultural inheritance resulting from behavioral plasticity (social learning).

Cultural evolution is becoming one of the most popular topics in biology as more and more scientists are beginning to notice how new behaviors can sweep through a population in less than a generation. The classic non-human example of this would be humpback whale songs changing year to year.

While cultural evolution occurs more quickly than genetic evolution in one sense, it also allows for genetic diversity to persist. Higher behavioral plasticity results in higher variety of trait and higher variety of preference for those traits. It can actually slow down evolution towards physiological adaptation for an environment by slowing the adaptation of physiological change. That being said, it can allow for more rapid adaption and by relying on social learning, only one or a few members of a population need to “discover” a new behavior for it to spread through the population.

It’s possible the mongooses have evolved this escort system as a way to maintain diverse foraging methods and reduce competition in their groups. Maintaining plasticity in foraging behaviors would be useful for social animals that have a wide variety of food sources, as the mongoose does.

Timon and Pumbaa: based on a true story

p02bk7tkSo admittedly Timon is a Meerkat not a banded mongoose, but it’s the same family so it’s close. In a cool example of mutualism, Warthogs (which, by the way, are awesome animals and don’t get nearly enough love) can rid themselves of ticks and bugs by getting groomed by mongooses.

Warthogs–which should look kind of scary to a small mongoose, actually get along quite well with them. Wild pigs tend to have quite a few ectoparasites and bugs inhabiting their skin/fur which can provide an easy snack for the banded mongoose. Warthogs have learned to lay down when mongooses are nearby, so they can pick off the parasites. Besides allowing mongooses to groom them, they also welcome vervet monkeys to snack on their ticks.

Mutualism between mammals is somewhat rare, but wild pigs and mongooses (and vervets for that matter) are highly intelligent and it shouldn’t come as much of a shock that they are able to enjoy the company of other species.

Mutualistic foraging between dwarf mongooses and hornbills

In another species of mongoose, the dwarf mongoose of the Taru desert often cooperatively forages with large birds, particularly hornbills, who share the same prey. The hornbills will wait to start foraging around termite mounds if the mongooses are sleeping and the mongooses will wait for the hornbills to be nearby to begin their foraging. This is true mutualism, as, while many animals have instances of exploiting each other’s coincidental presence for their benefit, the hornbills and dwarf mongoose actually plan their foraging activities around the other.

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The mongooses and the hornbills will warn each other of predators while they forage. The hornbills will even warn the mongooses when there are predators nearby that do NOT prey on the hornbills. The hornbills recognize predators specific to the mongoose as they will not warn against predators that do not prey on the mongoose. This is a pretty unique relationship as most cases of mutualism do not involve so much complex compensative behavior between species. The two species will communicate to one another with different vocalizations, and hornbills will sometimes wake up the sleepy mongooses when they’re impatiently waiting to start snapping up unfortunate insects.

Convergent evolution of neurotoxin resistance

Mongooses are mostly known for fighting cobras (partly because they’re exceptionally quick) but their resistance to the alpha-neurotoxin in cobra venom is what especially allows for this feat.

Acetylcholine is a very important neurotransmitter, so there are acetylcholine receptors all over your muscle cells that need to be free to bind (or not bind) acetylcholine, allowing your muscles to expand/contract. This neurotoxin, called alpha-bungarotoxin (alpha-BTX), works by binding to these acetylcholine receptors and blocking them up resulting in paralysis and eventually death. However the mongoose, the snakes themselves, and several other animals have independently evolved to alter the shape of their acetylcholine receptors so the neurotoxin, alpha-BTX, doesn’t bind.

Tweaks to the nicotinic acetylcholine receptor to prevent snake neurotoxin binding have been shown to have evolved at least four separate times in mammals (the honey badger, pigs, mongooses, and hedgehogs), but in the mongoose, the tweak involves a glycosylation site on the receptor matching the site present in snakes.

Syncing up birthdays

Despite being highly social and altruistic, meerkats are a more vicious member of the mongoose family and are especially well known to participate in infanticide. As meerkats live in a matriarchy with intense dominance hierarchies, many babies do not stand a chance from more dominant pregnant females. Banded mongooses however, have managed to evolve to sync up their birth so they’re all born on the same day. This prevents infanticide as all females are on essentially identical schedules (hormonally and in how they spend their time), so pups are never left alone with other females.

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Photo credit: Feargus Cooney

While most mammals have adapted to differentiate their own offspring very well, the banded mongoose benefits from having all pups be treated equally by the adult mongooses. Syncing up birth to the day or few days is a useful strategy, also seen in flamingos, where both male and female flamingos will even produce and feed crop milk to young who are not their own. However unlike flamingos, syncing up birthdays seems to be more about preventing infanticide and having a more lax dominance hierarchy.

This is a pretty unique strategy as usually species tend to fall on a continuum of high to minimal parental care. In this case, the banded mongoose receives a lot of “parental care” but not necessarily much from their parents. In almost all of nature, the level of paternal parental care is based on certainty of paternity, yet the mongoose has no idea who its close kin are. The behavior where a species mentors and takes care of young they know are not their own is, of course also seen in humans. Mongooses are exceptional in their array of cooperative behaviors– displaying reciprocity, altruism, cooperative breeding, and mutualism. But knowing humans, most will probably continue to believe we are special and entirely disconnected from these evolutionary adaptations.

Sources:

  1. Dwarf mongoose and hornbill mutualism in the Taru desert, Kenya. O. Anne-E. Rasa – Behavioral Ecology and Sociobiology – 1983
  2. How the mongoose can fight the snake: the binding site of the mongoose acetylcholine receptor. D. Barchan-S. Kachalsky-D. Neumann-Z. Vogel-M. Ovadia-E. Kochva-S. Fuchs – Proceedings of the National Academy of Sciences – 1992
  3. Decoupling of Genetic and Cultural Inheritance in a Wild Mammal. Catherine Sheppard-Harry Marshall-Richard Inger-Faye Thompson-Emma Vitikainen-Sam Barker-Hazel Nichols-David Wells-Robbie Mcdonald-Michael Cant – Current Biology – 2018
  4. Reproductive competition and the evolution of extreme birth synchrony in a cooperative mammal. S. Hodge-M. Bell-M. Cant – Biology Letters – 2010
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Bioluminescence- the immense diversity of organisms that glow

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Bioluminescence is a beautiful evolutionary phenomenon which has aided organisms in defending against predators, attracting mates, attracting prey, communicating, and even coping with metabolic stress. A ton of groups contain bioluminescent members (fungi, echinoderms, cnidarians, the list goes on and on) including some real evolutionary stand-outs.

In most cases (but not all!), bioluminescence results from enzyme-catalyzed oxidation of luciferins—light-emitting compounds—by luciferases. There can be many different luciferase compounds used even in closely related species.

New luciferin found in glowworms

A newly identified luciferin was discovered in caves in New Zealand (because of course it would be in a cave in New Zealand) in glowworms. This luciferin uses Xanthurenic acid and tyrosine as the two precursors to the glow. This particular glowworm is Arachnocampa luminosa, a species of fungus gnat that, in its larval stage, produces sticky threads by building a long muscousy tube and moving along the tube sort of vomiting up little sticky threads to trap insect prey. How disgustingly beautiful nature can be!

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Waitomo caves 

Glowworms are not really worms, but rather, larvae of several families of beetle and fungus gnat–however the bioluminescence is not homologous among the groups (so it’s arisen independently many times over). While it’s not always just the larvae that glows, the larvae emits the brightest blue-green glow. The glow helps the glowworms attract insects, attract mates, and protects them from predation (it also inspired James Cameron to make the blockbuster hit, Pocahontas with Glowworms Avatar).

Deep sea Cephalopods like to flash each other

An especially cool evolutionary example is of a deep-sea octopus, whose “suckers,” which still retain a sucker appearance and sucker-like traits, have had many of their muscle cells replaced with light producing cells. Researchers suspect this may have occurred as the result of once being a shallow-water bottom dwelling octopus, and moving to a deep open-ocean environment where suckers were less necessary.

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Deep sea octopus

Now it appears, the octopi use these glowing suckers for communicating to one another via visual signaling. They may also be using them for attracting a favorite prey item of theirs—copepods (small crustaceans). This is an unusual prey item for an octopus, but the copepods are attracted to the bioluminescence.

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Toyama Bay, Japan where firefly squid gather to spawn. Credit: Brian J. Skerry/Getty Images

For a more flashy light show, I’d recommend the firefly squid. Their deep blue lights (produced by photophores) are used for communicating with mates and perhaps rival squid. The light can also be used to break up the body pattern to confuse predators and attract small fish to prey on (because deep sea fish just cannot seem to learn which glowing lights mean danger). The really cool thing about firefly squid though, is not so much the light they produce, but the evolution of their eye that seemed to come with it. They are thought to be one of the only cephalopods to have color vision (by the way, cephalopod eyes: a fascinating topic). They have three visual pigments while other cephalopods only have one, and this may be so they can better distinguish ambient light from bioluminescent light, and perhaps because their light color is pretty unique from other bioluminescence emitted in the deep sea.

Symbiotic bacteria- lux operon helps flashlight fish and bobtail squid

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In perhaps the most of obvious function of bioluminescence: The flashlight fish (Anomalous katoptron in this case, though there are several species), produces light using symbiotic bacteria. The fish’s light organs are located under it’s eyes so it can turn the light on and off by blinking. These organs are packed with bioluminescent bacteria to produce a greenish-blue light. Researchers found that the fish blink less (meaning their organs are open) in the presence of their planktonic prey indicating they use their bioluminescence for finding prey.

 

Quorum sensing and a beautiful tale of symbiosis

One of my favorite bioluminescent evolutionary excerpts is that of Vibrio fischeri and Euprymna scollops (the Hawaiian bobtail squid). V. fischeri is a symbiotic bacterium that produces bioluminescence through the lux operon (which involves another luciferase oxidizing a compound to produce blue-green light). The Vibrio interact with the squid (using type IV pili) which starts the maturation of light organs in the squid. These bacteria help the squid conceal its shadow while its foraging for food under the moonlight. This protects the squid from predators while providing the bacteria with a stable home. 980x

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simplified diagram of lux operon at low and high cell density

What makes this bacterium especially notable, is that it was one of the first bacteria to be discovered to use quorum sensing. Quorum sensing is a gene expression regulation tool (often called “bacteria communication” and totally going to be on your exam tomorrow) where the Vibrio’s gene expression responds to changes in bacteria cell density. A signal molecule- N-acylhomoserine lactone (AHL), is synthesized by LuxI (a protein produced by the lux operon I mentioned earlier) and leaves the bacteria cells. LuxR forms a complex with AHL and binds the lux box causing the activation of luminescence genes. The bacteria colonize the squid’s light organ at a very high density producing lots of this AHL molecule.

Millipedes: Glow first used for coping with climate, co-opted for warning signal

 

If you’re ever in California, be on the lookout for the Motyxia millipedes. They’re pretty easy to spot as they emit a teal glow from their entire body. They also produce poison cyanide which many other millipedes do as well. Instead of concentrating their glow to one light organ and instead of emitting light from a luciferase reaction, they glow all over their exoskeleton using a photoprotein whose homology is unknown.

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M. sequoiae (left), M. bistipita (right)

But what’s REALLY cool about the Mytoxia is that for a while it was thought that bioluminescence evolved in the millipedes as a way to warn predators. However, when researchers discovered that another species (previously Xystocheir bistipita, now reclassified as Mytoxia bistipita) glows, but much more faintly, they looked more into it.

They found that Mytoxia may have actually evolved to cope with hot, dry climates (this species is found in the Sierra Nevada Mountains). The glow of M. bistipita is much less intense and they also have fewer predators than other species. Millepedes have difficulty metabolizing oxygen in hot, dry climates which creates toxic byproducts (like peroxide). Their bioluminescent photoprotein actually helps to neutralize these toxic byproducts. The researchers concluded that the millipedes colonized higher elevations more recently than the bioluminescence evolved, and that with that colonization came more predation. Only then did they co-opt the trait for warning predators of their poison cyanide production. The brighter the millipede, the more cyanide it contained!

Sources:

  1. Paul E. Marek, Wendy Moore. Discovery of a glowing millipede in California and the gradual evolution of bioluminescence in Diplopoda. Proceedings of the National Academy of Sciences, 2015.
  2. Jens Hellinger, Peter Jägers, Marcel Donner, Franziska Sutt, Melanie D. Mark, Budiono Senen, Ralph Tollrian, Stefan Herlitze. The Flashlight Fish Anomalops katoptron Uses Bioluminescent Light to Detect Prey in the Dark. PLOS ONE, 2017.
  3. Quorum Sensing in the Squid-Vibrio Symbiosis. Subhash C. Verma and  Tim Miyashiro. Int J Mol Sci. 2013 Aug.

Phytoestrogens aid flightless parrot- Soy will still not give men breasts

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Phytoestrogens are simply plant-derived xenoestrogens (mimics of estrogen). They’re abundant in legumes (soy, notably), but also present in many other plants. Despite their presence in certain plants being touted as scary, I’d say they’re pretty misunderstood.

Phytoestrogens help breeding success of kākāpō, the flightless nocturnal parrot

The darling flightless parrot of New Zealand has a struggling population partly because it only breeds once every few years. They seem to only breed during mast years (when plants produce a ton of edible fruit/seeds) and seek out fruit from the native rimu tree, which suggested the birds breeding success may rely on the presence of phytoestrogens found in the native plants. The hypothesis is that kākāpō don’t produce enough estrogen to make a fertile egg but the phytoestrogens act as supplements.qjjo1oz4sopgxokvcjww.jpg

The scientist conducting this study tested the native plants for estrogenic content and found high levels of phytoestrogens. They looked at the ligand binding region of the progesterone receptor, the androgen receptor, the estrogen receptor 1, and estrogen receptor 2 in four native parrot species, and non-native parrots and compared them with chicken receptors. They found that in most receptors there was more then 90% homology except in the estrogen 1 receptor. Parrot estrogen receptors are actually genetically different, containing an extra 8 amino acids in the hormone binding region, which changes the binding strength to estrogen.

Soy probably pretty good for you

Screen Shot 2017-07-30 at 11.12.05 AM.pngActive compounds of soy include isoflavones- daidzein, genistein, and glycitein. They act as phytoestrogens, a word which seems to frighten some people. A popular belief amongst anti-soy people is that men who ingest too much soy are going to re-enter puberty and turn into estrogen-filled feminized men (heaven forbid).

But this is not really what’s going on.

Phytoestrogens are structurally similar to estradiol so they have the ability to cause either estrogenic or antiestrogenic effects by blocking estrogen receptors. Phytoestrogens have weak estrogen activity in your body, so they may also bind weakly to estrogen receptors. They don’t displace estrogen, they supplement it.

Plants like soy have evolved phytoestrogens to protect from harmful microbes and to help form nitrogen-fixing root nodules.

So the expectation is that they act like antiestrogens in high estrogen concentration environments, and act like estrogen in low estrogen environments.

There are actually a lot of different estrogen receptors in the human body so the same chemical could be and agonist on one estrogen receptor type and an antagonist on another. So the phytoestrogens in plants could trigger an increase or decrease in endogenous estrogen through feedback loops.

It is almost certainly a serious oversimplification to say phytoestrogens are estrogen mimetics. Lots of compounds have partial agonist activity, meaning that at one concentration they are agonists and at a different concentration they are antagonists. It is possible they could affect the different receptors differently.

Reasons to even get excited over Phytoestrogens

Certain hormonal cancer (uterine, prostate, breast etc.) risks could possibly be lowered with phytoestrogen consumption. If they do actually compete with and block estrogen (an antagonist) at estrogen receptors in the breasts, cervix, or uterus, or if they depress estrogen production, they could tend to inhibit estrogen dependent tumors.

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Phytoestrogens may even provide some sort of benefit to women undergoing menopause and experiencing hot flashes, and post-menopausal women at risk for developing osteoporosis and issues in cognitive function which can sometimes be experienced due to dramatic hormone changes.

If phytoestrogens are agonists at estrogen receptors on osteoblasts and osteoclasts they will help reduce osteoporosis. These estrogen receptors are quite different from the receptors on breast tissue.

From a meta analysis on the effects of isoflavones on bone mineral density in menopausal women: “Isoflavone intervention significantly attenuates bone loss of the spine in menopausal women. These favorable effects become more significant when more than 90 mg/day of isoflavones are consumed. And soy isoflavone consumption for 6 months can be enough to exert beneficial effects on bone in menopausal women.”

Soy phytoestrogens are associated with much less negative effects than synthetic endocrine disruptors. And while results of most of these soy studies are dubious—varying with age, level of consumption, and the composition of the individual’s intestinal microflora, soy studies are just as well supported as pretty much any other “eat/drink more of (vegetable, tea, “superfood” etc) and (some health benefit) happens” claims.

While most people tend to be skeptical of simply ingesting a plant and deriving benefits (especially when they are comparing the plant to the highly powerful and concentrated drugs we’ve developed), underestimating and understudying plants has brought about, and continues to bring about, death and illness to plenty of people. So maybe it provides small benefits, but at the very least research does seem to have debunked the myth that soy is dangerous for people.

Constituents of soy if you’re still worried

 

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  • Protein
  • Oil- large amounts of polyunsaturated fatty acids (i.e. linoleic acid (omega 3))
  • Carbohydrates
  • Vitamins and minerals- K, P, Ca, Mg, Fe, B-Vitamins, antioxidants
  • Isoflavones
  • Phytosterols– Disogenin –sterol- is converted to progesterone in body
  • Phospholipids
  • Saponins*- being looked at especially
  • Ferritins- Soybean is a good source of iron
  • Phytic acid
  • Glyceollins- antiestrogen activity
  • Lunasin- peptide

Sources:

  1. Unique oestrogen receptor ligand-binding domain sequence of native parrots: a possible link between phytoestrogens and breeding success. Catherine E. J. Davis A , Adrian H. Bibby A , Kevin M. Buckley A , Kenneth P. McNatty A and Janet L. Pitman. 11 July 2017.
  2. 2014 Jul 7. Do soy isoflavones improve cognitive function in postmenopausal women? A meta-analysis. Cheng PF1, Chen JJ, Zhou XY, Ren YF, Huang W, Zhou JJ, Xie P.
  3. 2003 Jan-Feb. Effects of soy and other natural products on LDL:HDL ratio and other lipid parameters: a literature review. Hermansen K1, Dinesen B, Hoie LH, Morgenstern E, Gruenwald J. .
  4. Soy intake and risk of endocrine-related gynaecological cancer: a meta-analysis. Myung SK, Ju W, Choi HJ, Kim SC; Korean Meta-Analysis (KORMA) Study Group.
  5. Soy intake and cancer risk: a review of the in vitro and in vivo data. Messina MJ1, Persky V, Setchell KD, Barnes S.
  6. 2014 May 28. Effects of isoflavones and amino acid therapies for hot flashes and co-occurring symptoms during the menopausal transition and early postmenopause: A systematic review. Thomas Ismail, Taylor-Swanson Cray, Schnall, Mitchell, Woods
  7. Clinical studies show no effects of soy protein or isoflavones on reproductive hormones in men: results of a meta-analysis. Hamilton-Reeves JM1, Vazquez G, Duval SJ, Phipps WR, Kurzer MS, Messina MJ.
  8. Soy isoflavone intake increases bone mineral density in the spine of menopausal women: meta-analysis of randomized controlled trials. Ma DF1, Qin LQ, Wang PY, Katoh R.
  9. Soy isoflavones for osteoporosis: an evidence-based approach. Taku K1, Melby MK, Nishi N, Omori T, Kurzer MS.

Platypus venom- weird and unique, as expected

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“Do you think God gets stoned? I think so — look at the platypus.”

-Robin Williams

Venom isn’t very special in the animal kingdom, but our anthropocentric mindsets tend to focus more on large mammals than anything else, so to us it seems pretty mystical. Only a dozen or so mammals deliver venom, almost all of which deliver it via a bite for defense or predation. The platypus is unique in that it is so far the only animal known to use venom for a purpose other than defense or predation.

Only the male platypus has venom. And the male platypus only seems to have potent venom seasonally. The season when they have a lot of venom is unsurprisingly mating season, as the males actually use their venom, injected via venomous spurs on their hind legs, for intraspecific competition with other platypus males to keep territories and mates. While technically the echidna has venom, it can’t erect it’s spurs, and simply excretes a milky secretion.

platypus-spur-png.pngTheir venom, though nonlethal, causes excruciating pain for hours or days and is essentially nonresponsive to morphine. Only nerve-blocking agents (or antivenom) can provide relief.

A 2010 study found 83 peptides in platypus venom, many of which resemble venom genes from snakes, sea stars, and spiders. The platypus and reptiles have independently co-opted the same genes for venom usage making the platypus venom a cool example of molecular convergent evolution.

And just so the monotremes can continue to follow their pattern of general nonconformity and being surprisingly different from each other, the echidna venom gland transcriptome looks very different from the platypus one. You can read this post on their weird sex chromosomes for more.

The venom induces Ca2+ influx in cells, which results in neurotransmitter release. Defensin-Like peptides (defensins being immune proteins that usually defend the host from microbes), C-type natriuretic peptides (OvCNPs), nerve growth factor (OvNGF), and hyaluronidase have also been found. These peptides cause muscle relaxation, inflammation by promoting histamine release, and form ion channels in the lipid membranes of cells. The venom also contains a D-amino acid (as opposed to just all L-amino acids, which is the isomer previously thought to be the only conformation manufactured by cells).

First venomous animals were mammals
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Artist interpretation of Euchambersia mirabilis

The platypus having venom and laying eggs isn’t even that weird, as it seems to be that that was the norm for the ancestors of mammals. Euchambersia mirabilis, a therocephalian therapsid from the end of the Permian (~255 mya), which were some of the “almost-mammals” (the term “mammal-like reptile” is horribly outdated and silly but for some reason people still use it), was determined to have venom glands. Venom glands which appeared way before snakes and lizards evolved them, and actually millions of years before any snakes even existed.

bk9781849736633-00001-f1_hi-resSo while venom in mammals is very rare now, it may actually be an ancestral characteristic. Venom relatively expensive to have as it requires some method of injection into another animal, a gland, and then the making of proteins. It’s also suspected to be expensive because the loss of venom in animals that are no longer under pressure to produce any, is very common. Venom has a weak phylogenetic signal—similar types of venom are not necessarily found near each other on a phylogenetic tree, so genetically it seems not very “difficult” for various venoms to arise.

Monotreme venom as diabetes treatment?

The hormone, glucagon-like peptide-1 (GLP-1), is secreted in the gut, stimulating the release of insulin to lower blood glucose. But GLP-1 typically degrades within minutes in humans.

People with type 2 diabetes can’t maintain a normal blood sugar balance, but maybe they could if they had a less rapidly degrading GLP-1.

However in the platypus, there’s conflicting functions of the GLP-1. Not only is it a regulator of blood glucose in the gut, it is also in their venom. This conflict between the two different functions has resulted in the evolution of a dramatically changed GLP-1 system. GLP-1 in monotremes is resistant to the rapid degradation that occurs in other animals, and degrades by a completely different mechanism.

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GLP-1 and diabetes relationship

The function of GLP-1 in the venom seems to have resulted in the evolution of a stable form of GLP-1 in monotremes. Stable GLP-1 molecules can potentially be used as a type 2 diabetes treatment.

Both platypus and echidnas have evolved the same long-lasting form of the hormone GLP-1 despite echidnas not having spurs.

 

Sources:

  1. Kita, Masaki, David Stc. Black, Osamu Ohno, Kaoru Yamada, Hideo Kigoshi, and Daisuke Uemura. “Duck-Billed Platypus Venom Peptides Induce Ca2 Influx in Neuroblastoma Cells.” Journal of the American Chemical Society50 (2009)
  2. Enkhjargal Tsend-Ayush, Chuan He, Mark A. Myers, Sof Andrikopoulos, Nicole Wong, Patrick M. Sexton, Denise Wootten, Briony E. Forbes, Frank Grutzner. Monotreme glucagon-like peptide-1 in venom and gut: one gene – two very different functions. Scientific Reports, 2016
  3. Julien Benoit, Luke A. Norton, Paul R. Manger, Bruce S. Rubidge. Reappraisal of the envenoming capacity of Euchambersia mirabilis (Therapsida, Therocephalia) using μCT-scanning techniques. PLOS ONE, 2017