New paper: Plants and their very variable sex lives.

Plants mate. In a manner far more elegant than our own mammalian shenanigans, and far more important for the ongoing survival of the Earth’s ecosystems, plants are out there constantly having sex. And it is a deeply interesting thing involving insects, and wind, and stigmas, and stamens, and enough puzzling evolutionary biology to fill journal articles and occupy a small handful of academic careers.

My latest paper is about plant mating, and rather than wade through meadows of blooms to collect the data for this effort, I remained desk-bound in Milwaukee, wading through 30 years of plant mating literature with the intention of assembling a dataset to help us see plant mating in a new light.

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A mint-bush (Prostanthera lasianthos), caught in the act of mating.

As you may know, the flowers of many plant species are hermaphrodite, i.e. they bear both male and female sexual organs. This means plants can have sex with themselves. It’s called self-pollination, or “selfing”, and it can happen in two ways. First, pollen can move from the male parts of a flower to the female parts of the same flower. Second, on a single plant, pollen can move from the male parts of one flower to the female parts of a different flower.

“But isn’t this inbreeding??” I hear you ask, recoiling in horror at the moral and population genetic gutter down which I have so suddenly led you. Yes! Seed fertilized in a selfed flower is about as inbred as it gets, even more so than sibling mating. But you see, inbreeding is not always a bad thing—in fact inbreeding can actually be beneficial in some circumstances—and here’s where things get messy.

Genes are selfish. As such, they will do whatever it takes to get themselves propagated into another body. Consider then the selfish genes of a mother plant, which want to get into the next generation, and into as many individuals as possible. If a mother plant mates with a genetically different plant (an “outcross” mating event), its seeds each inherit approximately 50% of the mother’s genetic variation. This is because they combine with (and are diluted by) the genes of the pollen donor during pollination and sexual reproduction. On the other hand, if a mother self-fertilizes its own seeds, it transmits closer to 100% of its genetic legacy into each offspring. In the eyes of natural selection, this is a huge difference, and offers a great advantage to selfing over outcrossed reproduction.

So why aren’t all plants selfing all the time? This is because the huge advantage in transmitting genes via selfing is offset by the drawbacks of inbreeding. You can’t often get away with inbreeding without cost, and the cost is that inbred offspring are commonly less fit than their “outbred” siblings. Called “inbreeding depression”, this occurs because breeding from related individuals vastly raises the probability of combining rare genetic variants that harm the individual they are in. In the long run, inbreeding also reduces genetic variation that is essential for adapting to changing environments.

Evolutionary biologists have been pondering this tension for decades, and it led to the hypothesis that plants should be driven by natural selection into two polar opposite strategies: selfing plants should be favoured by natural selection when inbreeding depression is weak, and outcrossing plants should be favoured by natural selection when inbreeding depression is strong. Anything in the middle should not be adaptive, and should therefore be rare in nature. Sounds sensible, except numerous studies have now measured selfing/outcrossing across hundreds of plant species, and there is a curious and difficult-to-explain preponderance of plants that are neither exclusively selfing or outcrossing. These plants are having it both ways, seemingly hedging between strategies, and we call them the “mixed maters”.

Now for the problem my study addresses… Over the last 30 years, loads of studies have been measuring the selfing/outcrossing rate of plants in the wild. There have also been important studies which collect all these outcrossing estimates into big global datasets and generate observations like the one above: that mixed-mating is inexplicably common. For 30 years however, much of this discussion on global patterns was centred around average outcrossing per species, and using this to classify a species as a “selfer”, “outcrosser”, or “mixed mater”. We know evolution doesn’t work on a “species level” though. What is more appropriate is what is happening in a population context. And perhaps by averaging away all the variation within each species, my co-authors and I thought we might be missing an important perspective on the data.

What my co-authors and I did then was to collect all the outcrossing estimates from published papers containing three or more population outcrossing estimates. Going back 30 years, we collected data for 105 species and measured the variation in outcrossing within a species, among populations.

What we found was huge variation! There was commonly so much variation in mating within a species, that species averages felt inadequate for expressing where mating system variation lies. The data also showed that variation was difficult to predict. For example, there was an old hypothesis floating about that wind-pollinated plants were less variable in their outcrossing/selfing rate than animal pollinated species. The reason being that animals were thought to fluctuate more in their abundance and service between sites and seasons, while wind was a more consistent, reliable force for pollination. For the first time we were able to test this, and our analysis did not support the hypothesis. We also tested whether mating variation was evolving in a predictable fashion, but found that the relationship of plant species had no bearing on the variation we found in those species’ mating patterns.

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Arabis alpina: revealed in our study as a species with one of the most variable mating systems measured. By Hedwig Storch CC BY-SA 3.0, from Wikimedia Commons.

Ultimately, our study can’t solve the mystery of why we have so many mixed-mating plants. What it does do though is present a new way to look at the known range of variation in plant mating. There are other analyses waiting to be done with the data collected here, and we have highlighted where more studies are needed to answer interesting questions. For example, do different kinds of animal pollinators result in more or less variable outcrossing? Or do populations on the fringe of a species’ range experience more or less variable outcrossing?

As the body of knowledge on plant mating systems continues to grow, this dataset will grow too, and this population-level perspective on plant mating will hopefully provide the basis for the next insights into evolution’s influence on plant mating.

 

Full reference:

Whitehead MR, Lanfear R, Mitchell RJ, Karron JD. (2018) Plant mating systems often vary widely among populations. Frontiers in Ecology and Evolution, 6:38.

Further reading:

Goodwillie C, Kalisz S, Eckert CG. (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu. Rev. Ecol. Evol. Syst., 36:47-79.

Schemske, DW and Lande, R. (1985) The evolution of self‐fertilization and inbreeding depression in plants. II. Empirical observations. Evolution, 39:41-52.

Barrett, SC and Harder, LD. (2017) The Ecology of Mating and Its Evolutionary Consequences in Seed Plants. Annual Review of Ecology, Evolution, and Systematics, 48:135-157.

Australia’s sexual swindlers.

Seduction. Pollination. Deception.

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I recently wrote an article for Wildlife Australia about Australian sexually deceptive orchids, their evolutionary biology, and historical and current research about them. You can download and read the article here: PDF. Thanks to Carol Booth for her collaboration and editorial guidance.

The latest of Australia’s sexually deceptive orchids that I have seen (below) are Caleana major, the Flying Duck orchid (left), and a spider orchid Caladenia clavigera (right). Both were photographed last week in Brisbane Ranges NP, Victoria.

Flowering this year is one of the best seasons of recent times both east and west of the country. So if you’re in Australia, don’t miss the chance to get out bush and enjoy it.

Sex, lies and pollination. Australia’s remarkable sexual swindlers.

Article reposted from original publication with The Territories.

Rather than luring its pollinator with the promise of food this flower uses an equally, if not more, powerful motivator: sex.

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In shades of dusky green and claret red, the bird orchid’s subdued palette hints at its alternative lifestyle. The usual strategy for flowers attempting to catch the compound eye of a passing insect is to advertise proudly. Petals are used as panels for saturated colour, assembled en masse into conspicuous aggregate displays exuding exotic scents. In this way, nectar-filled flowers loudly broadcast the promise of their reward to entice would be pollinators into servicing them.

 

A deviant among flowering plants, the bird orchid eschews these typical hallmarks of floral advertisement. Crouched modestly on the forest floors of eastern Australia, its stature belies its status as one of the supreme specialists amongst the world’s flowering plants. Like those other showy flowers, the bird orchid needs the service of a pollinator from time to time, however unlike most other flowers, it attracts its pollinator without the payment of any reward. The orchid flower in fact completely lacks nectar.

 

Rather than luring its pollinator with the promise of food this flower uses an equally, if not more, powerful motivator: sex. Undetectable to human senses, the orchid’s advertisement is a precise chemical mimicry of a female wasp’s sex pheromone. This is targeted marketing at its finest, as the use of a signature sex pheromone ensures that the orchid attracts only males of a specific species of wasp.

 

Skimming by on wide zig-zagging flights, the wasps are interminably attracted when the ruse takes hold. They alight onto the flower with fervor, probing and hunting for the mate that their senses scream must be there. Bucking back into the column of the flower (the reproductive parts of an orchid flower are fused in this special structure), they make contact with the anthers and a large packet of pollen is deposited on them. The wasp disengages eventually and leaves, but soon, elsewhere, he will catch on the breeze the smell of a mate, and if fooled again, fulfill his role as duped courier for an orchid’s reproductive ends.

 

Called “sexual deception”, this mode of pollination was noticed by Darwin and his contemporaries in an age in which Europe’s natural sciences were in full bloom. It was a naturalist in Blackburn, Victoria however, who was first to discover the phenomenon outside Europe. In 1927, Edith Coleman had turned her great capacity for observation of the natural world to a peculiar native orchid. Resembling more flesh than flower, Cryptostylis, known also as “tongue-orchids” had caught her attention for its magnetic allure to a specific kind of wasp. Through her observations, Coleman was able to discern that male wasps were being attracted to the flower in order to copulate with it. An experiment through a window showed scent to be the primary attractant, and Coleman even observed the ejaculate remaining after having been visited by clearly convinced wasps. She wrote up her notes in a series of papers for the Victorian Naturalist and Transactions of the Royal Society for Entomology, which made quite a splash with the best of botany at the time.

 

We now know this was the tip of the iceberg. Australia is not only home to tongue orchids, but hosts a diverse array of other sexually deceptive orchids including the spider orchids, elbow orchids, hammer orchids, dragon orchids, greenhoods, duck orchids, hare orchids, beard orchids, bird orchids, and the list goes on. Harbouring over 50% of the world’s known examples of sexually deceptive pollination, Australia is certainly the world’s hotspot for this unusual phenomenon. Remarkably, we have several hundred species that employ this unique brand of pollinator attraction, and what is more remarkable, the evidence points to at least six different independent evolutionary occurrences in the Australian orchid family tree. To our eyes, sexual deception seems like a freaky, unlikely strategy and its repeated independent incidence through Australia’s evolutionary history is therefore a startling paradox.

 

Although the reliance on a single species of pollinator for pollination seems precarious, studies have demonstrated that sexual deception comes with the advantage of promoting healthy breeding for our native orchids. In nectar-bearing plants, foraging insects will frequently move between flowers on the same plant and between neighbouring plants. Called “optimal foraging”, exhausting local nectar supplies in a patch before putting energy into finding a new buffet makes economic sense for a nectar-feeding insect. Sexual deception however, has been shown to drive pollinators far from the flower after being fooled, so that pollen escapes the local neighbourhood. As a plant, your neighbours are likely to be related to you, thus deception is a way of ensuring offspring quality by avoiding breeding with your relatives.

 

Another factor supporting the profusion of our sexually deceptive species is Australia’s immense diversity of insects to fool. Although there are examples of gnat and ant sexual deception systems, wasps are the most commonly targeted pollinator for our orchids. Incredibly, we are only now beginning to uncover the immense hidden diversity of Australian wasps. For example, a recent study in a small patch of bush near Margaret River uncovered 28 species of wasps, most of which were previously unknown to science. With each of these species most likely having their own private sex-pheromone cocktail, there is seemingly a kaleidoscope of chemical communication channels available for different orchids to exploit.

 

Despite our deepening understanding of the natural history of sexual deception, its repeated occurrence in Australia remains a true puzzle.

 

Try the Atlas of Living Australia’s region search to discover which orchids (Plant family: Orchidaceae) live near you. [Link: http://biocache.ala.org.au/explore/your-area%5D

New article: The Territories

The Territories is Heath Killen’s new project. The site blends stories of Australia’s natural and cultural history under a unique aesthetic. I encourage you to check it out.

I was happy to make a recent contribution to The Territories, a story and photo gallery about Australia’s abundance of deceptive orchids:

“Sex, Lies and Pollination”

Rather than luring its pollinator with the promise of food this flower uses an equally, if not more, powerful motivator: sex. Undetectable to human senses, the orchid’s advertisement is a precise chemical mimicry of a female wasp’s sex pheromone. This is targeted marketing at its finest, as the use of a signature sex pheromone ensures that the orchid attracts only males of a specific species of wasp.

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Sex, Lies and Nectar: Evolutionary Biology as Written by Flowers

I spoke to the Canberra Skeptics group earlier this week, on a subject most near to my heart. The abstract appears below. It is my aim to soon turn elements of this into a video for online audiences.

In the eyes of evolution, finding a suitable mate for reproduction is one of the most critical stages in any organism’s life. The great majority of flowering plants have outsourced this essential service to animals, giving rise to a fascinating evolutionary dance between plants and pollinators.

Charles Darwin was the first to recognize that flowers were superb teachers of evolution. I will touch on his classic work and explain what we have since learned about remarkable flowers who smell like dung and death, flowers who attract insects with the false promise of sex and a fly with a ridiculously long tongue.

These and other awesome examples of floral evolution would surely have thrilled Darwin, and may even solve his “abominable mystery”: the rapid rise of the spectacular diversity of flowering plants.

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Male thynnid wasp gripping tightly to the lure of the hammer orchid (Drakaea glyptodon).

Pollination, evolution and an orchid’s seductive ruse.

In a PR coup for dumpy little green orchids everywhere, research from my PhD recently landed on the cover of the journal Evolution. But what is it about?

Spring. The Blue Mountains, west of Sydney. Altitude 1000m. Frosty winds whip a swaying eucalypt canopy infiltrated by billowing cloud. Down below, amongst snowgrass tufts, rotting logs and bracken dwell the diminutive bird orchids. Genus: Chiloglottis. They huddle in tight colonies, sporadically sprayed by the high country squall.

Each plant holds two leaves pressed flat to the damp ground. Between the leaves a stem rises, holding aloft a single intricate flower in dusky shades of green and burgundy. When banks of cloud give way to azure sky and the shrike-thrushes resume their piping, these small blooms become irresistible lures.

Their target are the gracile flower wasps. Slim glossy black insects, zooming silently on shimmering wings. They are helplessly drawn to the flower. The bird orchid is emitting a scent, detectable only to wasps, which signals the promise of a mate. Known as ‘sexual deception’, the elaborate ruse uses a precise mimicry of female wasp pheromones to fool male wasps into pollinating the orchid.

However, here on the forest floor there is not only one species of orchid outwitting wasps for its own reproductive ends. Look closer and slight differences in the characteristics of flowers and visiting wasps betray something more complex and interesting. There are actually two species here, looking largely the same, growing in the same places, both deceiving their wasp pollinators through the false promise of sex.

By emitting subtle variations of their chemical trickery, these orchids have “tuned in” to two different pollinator species. This research paper explores this phenomenon as a way of separating the gene pools of closely related organisms. At the heart of it, the story here is about the forces that keep species apart once they split, or reproductive isolation.

First, we show that the different pheromones emitted by the two orchids are responsible for attracting different pollinators. Through arcane powers of chemical synthesis that I do not understand, chemists created synthetic orchid pheromones for us. We took these into the landscape and showed that the two chemicals attract two different wasps. The only perceivable difference between the wasps involved is yellow spangles on the carapace of one of the varieties. What’s more, this specific attraction is exclusive. Chemical A only attracts wasp A, and chemical B only appeals to wasp B.

Next, we take real flowers of both kinds and place them in a row and watch the hapless wasps roll in. We see that wasp A is only attracted to flower A, even when flower B is present just centimetres away. The results are identical to the results of the synthetic pheromone experiment.

On the basis of scent, we therefore expect that orchid A may never mate with orchid B. Exclusive attraction ensures that despite living amongst one another, some orchids may never exchange genes. Despite looking almost the same to us, they may as well exist on separate islands. They distinct separate species.

In order to back this up we then looked at the genetics of the species. By using the same kind of genes used in human DNA fingerprinting we were able to show that the two kinds of orchid exhibit differences in their gene pools of a degree expected if they were different species. Furthermore, analysis showed not a single individual displaying the genetics of a hybrid. Our last tests were to make hand-pollinated hybrids to check that hybrids could indeed form. These crosses showed hybrid offspring germinated and grew faster than pure crosses.

The potential for animals to drive the formation of plant species has long been recognized. This study gives us a strong case study of how that process might look. Our orchids are spectacular examples of the power of pollinators to create and maintain plant species. Through selective pollinator attraction, the orchids have been set upon unique and separate evolutionary journeys.

Further reading:

Whitehead, M. R. and Peakall, R. (2014) Pollinator specificity drives strong prepollination reproductive isolation in sympatric sexually deceptive orchids. Evolution 68: 1561–1575. doi: 10.1111/evo.12382

Rod Peakall and Michael R. Whitehead (2014) Floral odour chemistry defines species boundaries and underpins strong reproductive isolation in sexually deceptive orchids Annals of Botany 113 (2): 341-355 first published online September 19, 2013 doi:10.1093/aob/mct199

Die Selfish Gene, Die.

I was recently asked by a friend for my opinion on David Dobbs’ piece “Die Selfish Gene, Die.” The article spins a yarn on why Richard Dawkins’ “Selfish Gene” thesis is sunk and the battle for updating it with a new theory of “genetic accommodation”.

It has attracted much attention as a great piece of science writing popularising the battle for a paradigm shift in genetics and evolution. Unfortunately its inaccurate and a bit too puffed up on its own bravado. My brief statement is below, however Jerry Coyne, Richard Dawkins and PZ Myers provide a more thorough commentary.

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Dobbs’ article describes a battle of two straw men. 

The term “genetic accommodation” is a new one to me, but the description of it sounds like phenotypic plasticity together with pleiotropy and epigenetics in a fancy jacket, but maybe we needed a word for that. Nonetheless, contrasting it with the selfish gene hypothesis is a false dichotomy. The messy truth for many traits lies somewhere in between, where the convoluted cascade of genetic-epigenetic-genetic interactions involved in “expression” will face selection as soon as its resultant phenotype hits the environment. 

The complexity of gene expression via interactions between genes and epigenetics (non-DNA inheritance) is blowing a lot of our heads off right now. It’s chaotically complex in there. I think the article therefore makes a mistake in referring to “gene expression” as a singular process.

Work I saw presented by John Mattick from the Garvan Institute provides a good example. Gene expression in human neurons can be governed by the interaction of RNAs, binding to “non-coding” DNA and interacting in 3 dimensions with complex protein molecules. In other words, it starts with a gene, which makes an RNA. That RNA’s action depends on the interaction between its sequence and where it binds on the genome. The sequence of DNA to which it binds, governs how it binds; simple like a zip, or more complex and looped up. Along comes a protein molecule (encoded earlier, elsewhere, by another gene) and the molecular properties of that gargantuan tangle of amino acids determine how it interacts with that looped up bit of RNA stuck to the DNA. This binding provides but a step in some long chain of protein interactions in a biological pathway. 

This kind of combinatorial complexity of interactions provides huge plasticity of action for a single set of tools (the genome).

One could argue that the first step of environmental interaction of any gene is the “environment” of the genome and epigenome it inhabits. This could still be squared with the selfish gene thesis.