New paper: The whimsical long-proboscid fly and its favourite colour.

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The flowers on one of these plants conceal drops of sticky nectar. The other is a cheating orchid, presenting empty flowers and false promises. Can you tell which is which? Even if you knew which one carried nectar, how can you tell the difference between them? The two plants might look a bit different to human high-res optics, but now try blurring your eyes. Pretty similar, huh?

What about this pair?

Screenshot 2018-10-30 15.09.50If it’s difficult for our brains and eyes to discern the difference between the flower with the reward and the one that’s falsely advertising, then what hope does a nectar-hunting fly with low resolution compound eyes and a smear of a central nervous system have?

Specifically, I’m talking about this fly…

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If this fly looks embarrassed, its because it has orchid pollen stuck to its face.

Until now, you probably thought lion, or elephant, or rhino were the most impressive animals roaming the grasslands of southern Africa. Well you’re wrong, and it’s ok to change your mind after seeing the majestic long-proboscid fly of South Africa. There are several species of these magnificent beasts, and this one is named Prosoeca ganglbaueri.

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That giant proboscis hanging from its face is a tool crafted by evolution for sucking nectar from the bottom of long flower tubes, and it can grow as long as 5 cm (which is longer than the fly’s own body length). Unlike butterflies who coil their proboscises, the long-proboscid flies simply hinge the instrument down, tucking it away underneath their bodies to trail out behind them. And this species isn’t even the most extreme: proboscises in Moegistorhynchus longirostris get up to 8 cm!

Sometimes handling that long instrument can be a challenge…

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In some areas of South Africa, P. ganglbaueri is the only creature capable of extracting nectar from flowers with very long floral tubes, and because of this it has become the exclusive pollinator for 20 species of plant. Altogether, the long-proboscid flies as a group bear the great responsibility as the only pollinator for approximately 130 species of plant, making them a truly important creature for the ongoing survival of many South African plants.

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Figure 1 from Whitehead et al. (2018): Prosoeca ganglbaueri feeding from a variety of nectar sources. (a) Zaluzianskya microsiphon, (b) Scabiosa columbaria, (c) Agapanthus campanulatus, (d) Dianthus basuticus.

An interesting fact about flowers that are pollinated by long-proboscid flies, is that most of them are pink, or white, or some variation in between (with one blue exception). This strong colour preference is a critical feature directing the evolution of the cheating orchid flowers introduced earlier. For a deceptive orchid to attract this fly, the orchids’ flower colour must match the flies’ colour preference, or the mimicry simply won’t work.

In my recent paper, we asked whether the colour preference of flies was something that they learned, like we learn to associate that perfect golden-brown hue of fried food with a mouth-watering culinary experience, or if it was instead a more hardwired innate response, like a moth drawn to a lamp. The answer is important for understanding ultimately what is driving the evolution of false advertisement signals in mimic orchids. So, for example, if flies had an innate bias to pink or white, then cheating orchid flowers would evolve to match that bias, in the same way that any good advertisements are designed to appeal to the fundamental desires of its audience. On the other hand, if flies learned to associate nectar reward with certain colours, their preference should be determined by the colour of their local nectar diet. Under the learned scenario, orchids should be evolving to match local flowers’ colours, not any intrinsic bias of the fly.

To test this, I took advantage of just how easy it is to bamboozle these flies. With a home-made artificial flower, painted to match the pink and white flowers visited by the fly, anyone can fool a fly into attempting to feed. So I mounted a pink and a white model to my “interview stick”, and travelled across the rugged Drakensberg Mountains to interview various populations of flies. In each location, I recorded whether the local flies preferred probing the pink or white model flower, as well as the colour and species of flower that the flies were using for nectar there.


The results were clear. Flies used to feeding mainly on pink flowers preferred the pink model. Flies that fed mainly on white flowers preferred the white model. And flies that fed on both pink, white, and violet flowers, showed no clear preference between pink and white.

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Figure 3 from Whitehead et al (2018): Pink-white preference for flies at seven sites. The x-axis shows colour preference, with pink on the right, white on the left. Measured preference at seven sites is represented, with the colour of local nectar sources depicted in the small pie charts.

This tells us that the flies are very flexible in their preferences, and the strong implication is that these flies are learning to associate colour and reward. A further result showed that as the variation of colours flies fed from increased, this made them less choosy in the pink-white preference choice. So the bottom line is that the colour of their local nectar-buffet strongly controls a fly’s colour preference.

What does this mean for orchid cheats? Well, the colour of nectar cheats is all important, and what matters most for the success of a deceptive orchid is the colour composition of the surrounding nectar-rich floral community.

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Post-script:
Still wondering about which flowers in the opening images were cheats, and which had nectar?

In both cases the deceptive orchid is on the left. The first image features Disa nivea (left), and Zaluzianskya microsiphon (right), the second features Disa pulchra (left) and Watsonia lepida (right).

Reference:

Whitehead MR, Gaskett AC, Johnson SD. (in press) Floral community predicts pollinators’ color preference: implications for Batesian floral mimicry. Behavioral Ecology 

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 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.