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.


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.


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.

New paper: Unearthing diversity in fungal dark matter

To be born an orchid is a most unlikely thing. First your parents must be pollinated, which is difficult. Orchids are both rare, and rarely pollinated due to the bizarre and dishonest means by which they go about attracting pollinators. Added to that, orchids often rely on a single species of pollinator to do the job.

Let’s say, however, that your orchid parents do manage to achieve fertilization. Your orchid mother will produce many thousands of tiny dust-like seed, which will be jettisoned into the wind. Unlike most seeds, you have no maternal energy investment to power your germination and first days as a seedling. Instead, you must rely on blind luck to land you within reaching distance of a strand of soil fungus. This fungus is the wet nurse to bring you into the world, invading the seed coat and hooking the young orchid up to a network of fungal strands that pervade the soil. Tapping into this network provides you with the first sips of carbohydrate and nutrient you need in order to build your first green leaf and begin to stand on your own roots. But it is not enough to land near any fungus. Many orchid species require fungal partnership with a specific species of fungus for this to occur at all. Multiplied together, it is a wonder that orchids ever overcome these odds to propagate themselves into the next generation.

The southwest of Western Australia is rightly famous as a global biodiversity hotspot. The area is particularly rich in orchids, and the spider orchids (Caladenia) are some of the most impressive and diverse of the region’s main orchid groups. In 1967, University of Adelaide researcher John Warcup discovered in association with Caladenia a new genus of fungi. Today those fungi are called Serendipita, and although we have known of them for around 60 years, there have been less than a handful of species discovered and described.


The spider orchid Caladenia arenicola was one of those sampled in the study


White spider orchid (Caladenia splendens)

Ubiquitous yet invisible

Although related to mushrooms, Serendipita fungi have not been observed producing the conspicuous spore-bearing fruit bodies we usually use to find and identify them. This makes them largely invisible, and I have therefore never observed them in the wild. Despite that, recent research using DNA sequencing has found them to be absolutely everywhere. Inside all kinds of plants, outside all kinds of plants, and distributed from the equator to Antarctica. It is clear then that there must be a hidden biodiversity of these species siting, waiting to be discovered.

My study took a wide sample of southwest WA spider orchid samples and assayed them for the presence of Serendipita fungi. We then sequenced the DNA of all the fungi we found, and used a new analytical technique for dividing that DNA sequence diversity into units that are probably species. This is currently the only way to sensibly identify Serendipita fungi, as they all look completely alike and do not produce spores in the lab.

We found a total of eight species of Serendipita fungi, including the original species discovered by Warcup back in the 60s. These came from a total of 18 species of orchid. At some sites where we sampled multiple orchid species, we found six species of Serendipita, meaning that the fungi were as diverse as the orchids!


Lying just below the soil horizon, that swollen, yellow stem bit is called the “collar”, and its where all spider orchids keep their fungus.

Untapped agricultural potential?

Although we have chosen to study these Serendipita in association with orchids, their wide host association has got other researchers interested in their role in plant health and application to agriculture. For example, Warcup’s species and one other have been used in experiments (and patent applications) showing inoculation with Serendipita results in profound benefits for the host plant, including:

  • Increased plant weight in maize, poplar, parsley, tobacco, barley, wheat, switchgrass and Arabidopsis
  • Enhanced grain yield in barley
  • Accelerated plant development in barley
  • Greater seed set, increased growth and faster flowering time in tobacco
  • Increased wheat yield in poor soils
  • Improved nutrient uptake in chickpea and lentil
  • Improved salinity tolerance in barley
  • Enhanced protection against root and stem pathogens in barley
  • Improved resistance to stem pathogens in tomato
  • Stronger defense response against mildew leaf pathogen in barley
  • Increased essential oil content in fennel and thyme

Figure 7 from Ray and Craven (2016): Root growth in winter wheat in Serendipita vermifera inoculated plants (left) versus control (right)

These proven benefits make Serendipita a potentially powerful tool to enhance plant productivity and stress tolerance in crops. Furthermore, application of Serendipita fungi could be an organic alternative permitting growers to lower the application of unsustainable and ecologically harmful synthetic fertilizers. Our knowledge of plant-Serendipita associations in the wild suggests that these relationships are more prevalent in nutrient poor soils such as those in southwest WA. They are probably one factor that allows our plant diversity to thrive in such weathered, poor soils. This means that species of fungi that have evolved with the nutrient poor soils (like those discovered in this paper) might be untapped tools to enhance agriculture taking place in those very same soils.


(Erratum: This story was edited to replace the figure attributed to Ray and Craven (2016). The first image I used was one showing Arabidopsis capability for mycorrhizal association. Arabidopsis is typically thought to be a non-mycorrhizal plant, which is why this is interesting. The image however showed slower growth in the mycorrhizal treatment. A related Serendipita has been shown to enhance root growth in Arabidopsis however. I have now updated the post with a more appropriate image of root growth gains in wheat. Thanks to Pawel Waryszak (@PWaryszak) for pointing this out.)


My study:

Whitehead, M. R., Catullo, R. A., Ruibal, M., Dixon, K. W., Peakall, R., & Linde, C. C. (2017). Evaluating multilocus Bayesian species delimitation for discovery of cryptic mycorrhizal diversity. Fungal Ecology, 26, 74-84.

Further reading:

Weiß, M., Sýkorová, Z., Garnica, S., Riess, K., Martos, F., Krause, C., … & Redecker, D. (2011). Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. Plos one, 6(2), e16793.

Weiß, M., Waller, F., Zuccaro, A., & Selosse, M. A. (2016). Sebacinales–one thousand and one interactions with land plants. New Phytologist, 211(1), 20-40.

Ray, P., & Craven, K. D. (2016). Sebacinavermifera: a unique root symbiont with vast agronomic potential. World Journal of Microbiology and Biotechnology, 32(1), 16.

Bokati, D., & Craven, K. D. (2016). The cryptic Sebacinales: An obscure but ubiquitous group of root symbionts comes to light. Fungal Ecology, 22, 115-119.

Australia’s sexual swindlers.

Seduction. Pollination. Deception.

Screenshot 2016-09-30 09.37.47.png
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 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.


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

Plant pollinator interactions in the South African flora

The slides from my recent departmental seminar at the ANU are below.

The first half of the talk concentrates on plant-pollinator interactions, floral guilds and floral evolution. The second half is a slideshow of vistas, creatures and plants I encountered in my work.

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.


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.