Heavy human harvesting of a valuable medicinal plant leads to evolution of new leaf and flower colors

November 22, 2020 • 10:30 am

If humans harvest an animal or plant, especially if they harvest it heavily, the species often evolves to make itself less “harvestable”.  For example, commerical fisheries that take the larger fish in the sea have led to the evolution of individuals that mature earlier at a smaller size, for it is the small reproducing fish who don’t get caught. Elephants harvested for their ivory have, in some populations, evolved smaller tusks or even tusklessness, for it’s the tuskless elephants who leave more offspring. (The condition for all such evolution, of course, is that the evolved conditions have at least a partial genetic basis.)

Finally, there’s a similar phenomenon called “Vavilovian mimicry”—named after the great Russian geneticist and botanist Nikolai Vavilov, who was imprisoned by the Soviets and died in the gulag because he dared to embrace Western genetics and science against the teachings of the charlatan Lysenko.

In Vavilovian mimicry, weeds are selected among agricultural crops with which they grow to get themselves in the next generation of the crop. Farmers have mechanical ways to sort out the weed seeds during harvesting, and this imposes selection on the weeds to produce seeds of the same size and shape as the crop; it’s those mutant weed seeds that get replanted the next year.

A cool and famous example is how the common vetch (Vicia sativa), a weed, has evolved in crop areas so that its seeds come to closely resemble that of the edible lentil (Lens culinaris), a crop that the weed infests.  Because lentil seeds, which are what’s eaten, are tasty but vetch seeds are bitter, farmers have used mechanical and visual sorting to discard the wild vetch seeds. Over time, the vetch seeds have undergone what’s called “unnatural selection” (for Vavlovian mimicry) to have the same size, color, and shape (flattened) as the lentil seeds. Here’s a diagram showing the cultivated lentils (A) along with the wild vetch seeds growing on their own (B), and the seeds of the same vetch, but which have grown in lentil fields. Look at the big evolutionary change in the vetch seeds!:

Today we have another example of plants mimicking other things—in this case the environment—to hide themselves from being harvested.  Fritillaria delavay, is a perennial alpine Asian plant that grows from a bulb, living about five years. The bulbs, particularly the small ones, are very prized in Chinese medicine, especially for treating tuberculosis, fetching up to nearly $500 per kilogram. (Since they’re small, it takes about 3,500 bulbs to make a kilogram.) They are picked visually, with harvesters looking for the bright green leaves and flowers of the plant that stand out against their rocky background.

Since harvesting is heavy, you can guess how the plant evolved. That evolution is documented in this new paper in Current Biology (click on screenshot below, or go here to get the pdf, both of which are free).  If you want a journalistic summary, there’s one in the Times and another in the Guardian.

In short, the plant has undergone evolution of both leaf and flower color to make it more inconspicuous and thus harder to find and harvest (harvesting, since it takes the bulb, kills the plant). You’re more likely to reproduce if you’re not seen, and in harvested areas those plants with mutations making them match the background better are those that survive. Herbivores apparently aren’t involved in this system, as nothing has been observed to eat the plant, which is full of alkaloids and toxic.

Here are pictures F. dlavayi in an unharvested area (left) and one in an area heavily harvested (right). You can guess which is which. Note the difference in the color of both leaves and flowers. In fact, the green color can evolve to either reddish, brownish, or grayish colors depending on the color of the background.

 

In the paper, the authors collected plants from eight populations in southwest China, and found significant divergence of color among the populations using a special “vision model” to measure the colors and luminescence seen by humans. Here’s a plot of the variation among the eight populations (each dot has a color that is related to the plant color, with each color representing a single population):

(From paper): Plant Color Variation of Fritillaria delavayi among Populations. (A) Color divergence from eight populations in human CIE L∗a∗b∗ color space

Are the plants camouflaged in their local area, and is the degree of the camouflage correlated with how heavily the plants are harvested? The authors derived a measure of how camouflaged a plant was by comparing leaf and flower color with the color of the soil or rock background (also measured using the human-vision algorithm). Collection intensity was assessed by questioning the locals and deriving an estimate of intensity = [amount of bulbs collected]/[relative abundance of the plant in the area]. The higher this fraction, the heavier the collection effort (i.e., the proportion of the population that gets taken by collectors).

As you see from the plot below, the higher the collection intensity in a population (position to the right), the better the mimicry (lower values on the Y axis). The relationship is highly statistically significant (p < 0.001). Clearly, the prediction that the color evolved in response to human harvesting is supported.

Finally, the authors looked at an ancillary relationship: that between the difficulty of digging up bulbs (some are hidden under dirt and rock piles) and the degree of camouflage of the population. The relationship they found is shown below. One predicts that the easier it is to dig up a bulb, the more camouflaged the population would be, for easier digging makes for heavier harvesting and thus stronger “unnatural selection”. The relationship below affirms the prediction, though they left out one population where collection is easy but the plant is green—yet collection isn’t heavy in this population. (This sounds like post-facto discarding of data, but could be kosher.)

Whether each dot is statistically independent of the others, which seems to be the assumption when doing the nonparametric correlations, is dubious, since plants in a given area are related to one another, and each plant didn’t evolve its color independently—the population as a whole evolved its color as a gene pool.

Leaving that possible quibble aside, the authors finally did a computer experiment on target slides showing plants matching their background to various degrees. They found, as expected, that the locals took longer to detect a plant when it matched the background, confirming that your chance of escaping “predation” is likely higher when you’re better camouflaged.

Here’s one more photo from the paper showing the cryptic nature of the plant in brown and gray backgrounds (C and D), and how readily the bright green plants stands out against a scree background (A and B; this is clearly a low-harvest area).

Plant Color Variation of Fritillaria delavayi among Populations

There are no new principles demonstrated in this paper, but the results are still fascinating, and show a mixture of artificial and natural selection that’s called “unnatural selection.” That is, the color isn’t a deliberate product of the breeder, like the grotesquely long bodies and minuscule limbs of wiener dogs, but is an inadvertent result of “artificial” selection. (I’m not even sure I’d call this artificial selection, for humans are part of nature and are gathering something they need.) And, like natural selection, all this process requires is differential reproduction of individuals that have different genetic variants.

If you want to read more about “unnatural selection” and how it’s affected many species, click on the screenshot below.

h/t: Ben, Matthew, Florian

_________________

Niu, Y., M. Stevens, and H. Sun. 2020. Commercial Harvesting Has Driven the Evolution of Camouflage in an Alpine Plant. Current Biology. Online. https://doi.org/10.1016/j.cub.2020.10.078

A beautiful planthopper that mimics an ant (with a twist)

July 17, 2020 • 10:00 am

Planthoppers are in the order Hemiptera—the “true bugs”—along with cicadas and aphids, and are in the suborder AuchenorrhynchaI’ve written about them before: they have all kinds of bizarre appearances that sometimes defy explanation (e.g., these ones).  In 2012 I wrote a report about a strange planthopper (Formiscurra indicus) that mimicked an ant, but the kicker was that the mimicry was described as being limited to one sex: the males. The females looked pretty much like “normal” planthoppers.

Sex-limited mimicry is known in some species, like butterflies, and I discuss it in my 2012 post, but there are reasonable (though untested) explanations for it. Some butterflies, for instance, have mimicry limited to females, with females of a single species varying in appearance across their range to mimic the local distasteful species (“Batesian mimicry“), but males look the same everywhere. That’s usually explained by sexual selection: females have a hardwired search image for males of their species, and while the females may change appearance based on local selection pressures to resemble distasteful “model” species, the males are prevented from doing so because they’d lose more in sexual attractiveness than they’d gain in protection from predation.

That 2012 article appeared in the Guardian (the report has disappeared) but there were no scientific papers describing it. Now, after seven years, one has finally showed up, in the Czech journal Acta Entomologica Musei Nationalis Pragae. Click on the screenshot below to see it and get a free pdf; the reference is at the bottom.

There are actually two species mentioned in this paper: Formiscurra atlas, found in Ethiopia, which was wrongly named in the Guardian report as Formiscurra indicus.  (The latter species, from India, had already been named in 2011.)  In the present paper, published in January of this year, the author (who co-wrote the 2011 paper) formally describes and names Formiscurra atlas, goes into great detail about its unusual morphology, and mention, though not in detail, the fact that in this species only the males are mimics—mimics of ants, or “myrmecomorphs”.

We can ignore the morphological details save that the species, in one sex only, is a mimic.  Here are pictures of a male and female. Fig 1 and 2 show the male, side and dorsal (top) view, respectively, while 3 and 4 show the female. The male has a round protuberance on its head (see the eyes behind it) that makes it look more antlike. The curious thing to me is that, according to the authors, they say that this ball-shaped protuberance evolved to resemble an ant’s abdomen, while to me, and in the pictures of its relative below, it looks like an ant’s head, while the male planthopper’s abdomen has evolved to resemble an ant’s abdomen. I’m not sure whether this is a mistake, but it’s at least clear that one sex but not the other has evolved to resemble an ant.

In Figs. 3 and 4 you see the female of the species, pretty “normal” for a planthopper. She does have a small cylindrical protuberance on her head that may be a vestigial remnant of the larger protuberance in males.

The authors, however, don’t say how they know that these are two sexes of the same species. DNA would tell, but no molecular analyses are described.

 

The authors also provide a photograph of a live specimen of the relative F. indicus, which is remarkably antlike, though I still say that in the first picture below (from the paper), as well as the second (from Wikipedia), the head protuberance is “supposed” to resemble the head rather than the abdomen of the ant:

From Wikipedia’s article on F. indicus. “Male climbing a twig.”

There remains only one thing to consider: why are only the males ant mimics? We know the benefits of ant mimicry, which I described in my earlier post:

Why mimic ants?  Ant mimicry is common in many diverse groups; in fact, Wikipedia has an article on it.  There could be several explanations for why the planthopper is such a mimic.  The mimicry could be aposematic, that is, the ants that are being mimicked are poisonous and distasteful, and predators have learned to avoid them.  By mistaking the leafhopper for an ant, the hoppers gain respite from being eaten, an obvious selective advantage.  Alternatively, the leafhopper could live in an ant colony and gain advantages that way, including protection by being in a group or getting access to the ants’ food. I find this less plausible since ants are good at sniffing out intruders.  And there are undoubtedly other possible reasons for mimicry.

I still think that the advantage of mimicry here is “Batesian”: that is, many ants are distasteful to predators like birds and lizards, as ants are full of poisons and other distasteful or toxic compounds, and very few species have them as a steady diet. If you’ve learned to avoid an ant, then a reproductive advantage accrues to any planthopper (planthoppers are tasty because they feed on sap and vegetation) that looks more like an avoided ant species. And there’s no evidence that these planthoppers are associated with ant colonies.

But on to the burning question: why is mimicry limited to one sex? If the mimics were females and the males were non-mimetic, we might explain it as we do in butterflies: males are constrained not to evolve because females retain the ancestral preference for how a mate “should” look. But in this case the mimics are the males and the females presumably didn’t evolve that much.  I don’t even want to speculate here (nor does author Gnezdilov), except to say that I’d like better evidence that these are indeed two sexes of the same species. Maybe I’ve missed earlier data on that.

_____________________

Gnezdilov, V. M. 2019. A new species of the myrmecomorphic planthopper genus Formiscurra (Fulgoroidea: Caliscelidae) from Ethiopia. Acta Entomologica Museu Nationalis Pragae. 59(1): DOI: https://doi.org/10.2478/aemnp-2019-0002  Published online:  24 Jan 2020

Readers’ wildlife photos

May 18, 2020 • 7:45 am

Today we have one of my favorite creatures—jumping spiders (“salticids”)—photographed by Tony Eales from Brisbane. His notes are indented below:

Jumping spiders.

I’m a big fan of ant-mimicking jumping spiders. Some of them have extreme modifications to the basic spider body plan as well as behaviours like holding their forelegs up to imitate antenna. However this is the first time I’ve seen this. This ant mimic Myrmarachne sp. imitates rattle antsPolyrhachis (Cyrtomyrma) sp. These are formicine ants, meaning they have no sting and instead spray a nasty formic acid chemical cocktail at attackers and prey. When threatened, they sling their abdomens underneath their body ready to spray anything that gets too close. This ant-mimicking spider seems to also be able to mimic this distinctive posture.

Males like this one are very easy to distinguish from ants, at least to our eyes because of the extraordinary long jaws. The females however are indistinguishable at a glance from the ants they mimic.

These male jaws are amazing sexual features. I had the good fortune to find a male the other day that seemed to be obsessed with opening and flexing its jaws, not something they tend to do for more than a quick second usually.

And remember: six legs ant; eight legs spider.

Look at those gaping jaws!

 

The ant:

JAC: A female. Note how their first pair of legs resembles the antennae of an ant:

JAWS!

I found another ant mimic, Myrmarachne cf bicolor, in my back yard. As you can see from this one on my finger, they are very small. These ants mimic strobe antsOpisthopsis sp. Again, not a stinging ant. In fact, we have a number of rather painful stinging ants, but I can’t think of any jumping spiders that mimic these ants. They always seem to mimic formicine ants.

Finally a few cute pictures of tiny juvenile jumping spiders having a munch.


Spot the antlion!

February 22, 2020 • 1:00 pm

Matthew sent this tweet which shows a cryptic antlion—the predatory larva of a neuropteran insect in the family Myrmeleontidae, whose flying adult looks like a lacewing. (The adults are much less well known than these predatory larvae, which I used to keep as pets as a child).

This is rated very easy, but we haven’t had a “spot the. . . ” feature in a while so have a look. It also shows you once again how remarkably good natural selection can be in matching animals to their backgrounds

Enlarged. See the big mandibles spread out, waiting to snap shut on a hapless victim?

Antlions like the one above are free-roaming, getting their prey on the hoof. But others, like the ones I used to keep, dig pits that trap unwary prey, similar to this one from a BBC Earth video. (I collected my ant lions from the dirt of vacant lots and put them in dishes to recreate their pits. Then I’d feed them ants. I am a bad person.)

Reader’s wildlife photo (and video)

February 16, 2020 • 7:45 am

As I reported, Andreas Kay, a superb photographer of Ecuadorian biodiversity, died last October at the young age of 56.  It was a tragic loss, but he left behind a big legacy: nearly 30,000 unpublished photos of insects and plants from Andean Ecuador. These were inherited by reader Lou Jost, a biologist who inhabits a field station in the Ecuadorian rainforest. Lou has promised to send samples of Andreas’s photos from time to time, so we’ll be able to enjoy them and remember the man.

What I didn’t know until Lou wrote last is that Andreas took videos as well, and very good ones (you can see his YouTube site here). Two days ago Lou sent me one of Andreas’s photos and a link to a video of the insect in the picture. First, the photo with Andreas’s caption:

These moss mimic Stick Insects (Trychopeplus thaumasius?) were filmed at Finca Palmonte near Baños in the cloud forest of Ecuador. During daytime they hang nearly imperceptible between moss covered twigs and only become active at night to feed on leaves. They not only look like moss but even move like waving in the wind. 

Can you spot it?

Now look at the video and see how the thing moves erratically. It shows that natural selection for mimicry can operate not just on appearance, but also on behavior. (Sound up).

Also from Andreas:

Watch two other videos of this species: https://youtu.be/vZPVeJhld_I and https://youtu.be/xCqqnu2Xk2M

I can’t help but add Andreas’s post from Facebook (forwarded by Lou) when he knew he was dying of a brain tumor. It always makes me tear up. A naturalist to the end. . .

A stunning case of mimicry

January 21, 2020 • 9:00 am

I don’t remember encountering this case of mimicry, but it’s so amazing that, when I became aware of it from a tweet (yes, Twitter has its uses), I decided to give it a post of its own.

First the tweet, sent to me by Matthew. He added, “This is the Iranian viper, as featured in Seven Worlds, One Planet, made by the BBC. Amazing.”

You don’t need to translate the Spanish, though, as the video below tells all. I swear that when I first watched it, I thought there was a real spider crawling on the snake’s back.

The snake is the spider-tailed horned viper, Pseudocerastes urarachnoides, which has a small range in Western Iran (map from Wikipedia):

It wasn’t described as a new species until 2006 in the paper below (free access); before that it was thought to be the already-describe Persian horned viper. (I guess they overlooked the tail ornament.)

Here’s a photo of the tail “spider” from the paper; the one below that is from Wikipedia. The resemblance may not be precise, but (as you see above), when the ornament is moved about, it looks remarkably like a spider—certainly good enough to fool birds.

In that paper, the authors didn’t know how the tail ornament was used, but were impressed at its spider-like appearance. And they guessed accurately:

This raises the question of the elaborate and sophisticated appearance of the caudal appendage in our new species, as the waving or wriggling motion of a distinctively colored tail tip seems perfectly adequate to attract lizard and anuran prey. We can only speculate that in the case of the present species, the caudal lure serves to deceive a more specific kind of prey, such as shrews or birds. Indeed, ZMGU 1300 [the specimen number] contains an undigested, unidentified passerine bird in the stomach (the feet protruding through the body wall).

Only later, using live captive specimens, did researchers see that the ornament did indeed attract birds that the snake caught and consumed, as in the video above.

Any biologist who sees this is immediately impressed by the ability of natural selection to mold not only morphology, but the behavior of the snake: the twitching of its tail so that the spider ornament appears to “walk.”  But any adaptation like this ornament must have incipient stages, and each subsequent modification must improve the adaptation—that is, it much give the snake possessing the “improved” improvement a reproductive advantage. (That advantage would derive from the better nutrition of a snake who caught more birds, and thus might have more offspring, increasing the proportion of genes for more spider-like ornaments.)

My own guess was that the ornament started with the simple twitching of the tail of an immobile snake, a twitching that might attract predators and, moreover, is already known in several snakes. After that, any mutation that modified the tail, making it look more like a spider, would give the snake a further reproductive advantage. And so we get the spider ornament, which might of course still be evolving. Concurrent with the evolution of the ornament itself would be the evolution of the snake’s tail-twitching behavior, which makes the caudal appendage resemble a spider nearly perfectly.

It turns out, of course, that I’m not the first person to think of this scenario. Discover Magazine wrote about this snake last spring, and speculated about its evolution:

“The evolution of luring is more complex than contrasting color or simple shaking — the movement is precisely adapted to duplicate prey movement frequencies, amplitudes and directions, at least in specialized cases.”It’s not uncommon for many snakes to do something similar with their tails to deceive prey. The common death adder of Australia buries itself in leaves, then writhes its tail like a worm to catch lizards and frogs. The Saharan sand viper conceals itself in sand with only its eyes and nostrils visible. When a lizard comes along, it sticks its tail out from the dirt, making it squirm like an insect larvae.  The behavior — and the elaborate body modifications that can accompany it — likely arose from a behavior common to many reptiles, Schwenk explains. When they are about to strike prey, any lizards and snakes enter a hyper-alert pose. The reptiles will focus their vision by cocking their heads to the side, arching their backs, and certain species will commonly vibrate their tail tip against the ground. This can distract the prey, which will shift its attention to the vibrating tail, ignoring the reptile mouth opening to grab them.“This simple pattern leads to selection causing refining of the tail form and motion to be more attractive to such prey by more accurately mimicking actual prey movements,” Schwenk theorizes. “The other ancestral condition that could have led to caudal luring, or possibly an intermediate step in the process, is the use of tail vibration for prey distraction rather than for luring.” Indeed, those most famous tail shakers, the rattlesnakes, sometimes also use caudal luring. For example, juvenile dusky pygmy rattlesnakes, whose rattle is so small it barely makes noise, wiggle their tails to attract prey. The behavior, in fact, may be key to how rattlesnakes evolved their distinctive rears, although this theory is somewhat controversial. “Like many other apparently simple things in biology, there is a lot of complexity to caudal luring that has barely been explored,” Schwenk says. “Much of this has been considered in a piecemeal fashion, but a thorough review and synthesis … has not been attempted.”

Now we’re not sure if this is the correct evolutionary pathway, but constructing a plausible step-by-step scenario like this, and showing that the intermediate “stages” occur as adaptations among existing species, is sufficient to refute the creationist claim that structures like the spider ornament could not have evolved and thus much have been created by God (or a “designer”, which means the same thing). The same kind of argument was used by Darwin in The Origin to refute Paley’s argument that the camera eye must have been created by God. Dawkins discusses it in the video below (and, as I recall, in his book The Blind Watchmaker).

 

Readers’ wildlife photos

January 10, 2020 • 7:45 am

Down in burning Australia, Tony Eales has managed to photograph some of the insects that haven’t yet been incinerated. Note that there is some mimicry as well as crypsis (camouflage) in the photos below. Tony’s notes are indented:

Today is a mish-mash of recent things that may be of interest.

Last year I photographed a female Clear-wing Persimmon Borer (Ichneumenoptera chrysophanes), a beautiful wasp-mimicking moth whose larvae bore into the stems of certain fruit trees. My first photograph of the new decade was of the male of this species. I was having friends over for a BBQ on the first of January and I was standing around talking when, out of the corner of my eye, I noticed something odd looking on a leaf. I announced loudly “I have to get my camera” and ran off to the office, came back and got the shot.

Next a couple of possible wasp-mimicking Stiletto flies. I say possible because the first one, Agapophytus aterrimus, certainly has some of the wasp-mimicking characteristics but also is reminiscent of some Jewel Beetles in the genus Castiarina:

Castiarina sp:

The second wasp-mimic is more straightforward. The fly Agapophytus pallidicornis is a striking mimic of the common spider-wasps in the genus Fabriogenia. In fact, when I photographed it, the only clue I had that I might be dealing with something other than a spider-wasp was that it was sitting still, whereas spider-wasp’s restless searching for prey never seems to pause for even a  second.

Fabriogenia sp.:

I finally got to photograph the Giant Bulldog Ant (Myrmecia brevinoda). It was a hulking 35mm long and not at all impressed with me. They’re a terrifying ant to play around with, they’re fast defensive and have excellent eyesight and reportedly an unbelievably painful sting. Even so I messed with this one a lot to make sure I got the shot. The only bigger ant in Australia is the queen of this species which can be over 40mm long.

I found the larvae of a species of Tortoise Leaf Beetle which I think is probably Aspidimorpha deusta. The larvae in this family are unusual for carrying around a “faecal shield” made up of excretions, poisonous chemicals from the plants they eat and shed exoskeletons. A. deusta tend to hold the shield over them like an umbrella.

From mimicry to defence to camouflage. I’ve been finding these transparent and green cockroaches on the underside of leaves in the local rainforest. They are in the genus Mediastinia and they have exoskeletons so transparent that from certain angles it simply doesn’t show up in photographs.

Also in the rainforest I found a tiny Pygmy Grasshopper in the family Tetrigidae. They’re only a couple of millimetres in length as adults and well camouflaged as  a piece of moss that they’re very easy to miss.

But of course no stings, or camouflage or mimicry can defend an insect from fungal parasites like this Ophiocordyceps that I found after having consuded what looks like some sort of Hoverfly.

On the climate apocalypse front, the fires are still raging with no real end in sight as we come to the hottest end of the traditional fire season (note these fires have been burning since September), the latest estimates are that 10 million hectares have burned leading to the loss of an estimated one billion “animals” (and you know they’re only talking about the vertebrates). While these fires and the loss of lives, homes and forests is rightly the big news, as bad as they are, the devastation from unusually warm ocean temperatures on tropical reef systems is even worse.

That story is only just coming out now but we’ll be counting the cost for decades to come. On my way to my favourite little rainforest patch I was horrified at the state of the surrounding forest. This moist eucalyptus forest looked like it had already been burned but you could see that it wasn’t. It was that every young tree was dead from drought and all the older trees had dead limbs and drooping dry foliage. This kind of forest has rare and low intensity understory burns and it protects the rainforest that it surrounds; however in these conditions one can easily imagine a fire getting into the dry crowns and wiping out everything.

All we can do is cross our fingers and wait for rains and hoping nothing sets it off beforehand.