New paper: The whimsical long-tongue 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 

Photos from the field: Northern Sand-plains, WA

Peaceful woodlands of widely spaced gnarled Eucalypts lie in mosaic with spiny, scratchy, shrubby heath on the sand-plains north of Perth. They form one of the most floristically diverse regions on earth, with estimates of over 60 species of plant per 0.01 ha (an area smaller than half an an IMAX screen).

With so many species packed on top of one another, it is perhaps not surprising that in the effort to co-exist, some plants have been forced to flower outside the traditional Spring-flowering window. Winter in the sand-plains, while often wet and cloudy, is therefore anything but dull. While daily insect activity is very low, resident birds and honey possums must still feed, and so there are a comparatively high number of vertebrate-pollinated species in full flower at this time of year.

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Omphalina chromacea in its diminutive but sulphureous glory

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Bird-pollinated Astroloma glaucenscens excludes insect visitors with a tiny corolla-tube opening

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Pterostylis sanguinea: a sexually-deceptive trap-pollination orchid

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Astroloma stomarrhena, bird-pollinated. This individual has curiously short corolla tubes.

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Calothamnus sanguineus mixed in with Conostephium

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Calothamnus sanguineus

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An early-flowering Caladenia latifolia

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Diuris corymbosa

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Tiny pgymy Drosera

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One of the most common orchids in the area, but I’ve never seen it flower. Pyrorchis leaf.

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Very rare, and while this specimen is a little tired late in the season, the winter-flowering Cleopatra’s Needles (Thelymitra apiculata) is a stunning contrast of hues.

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.

First video of bird pollination in Astroloma stomarrhena

I’m thrilled to share this never-before seen sequence of birds feeding on Astroloma stomarrhena, a winter-flowering shrub endemic to Western Australia.

Earlier this year, I decided A. stomarrhena looked like a perfect candidate for my new study on pollinators and gene flow. What I needed was a bird-pollinated species of plant, closely related to an insect-pollinated species. This one seemed to match all the criteria I needed, except there was no evidence that it was bird-pollinated. But with those long, tapered corolla tubes, and that pink-red coloration, I believed that birds absolutely had to be the pollinator.

The danger was, that while birds might be visitors, the plant could be somewhat “generalized”, and also use insects. This is pretty common, especially in places like Australia where European Honeybees (Apis mellifera) have invaded ecosystems that evolved in their absence, and honeybees will visit absolutely everything whether the plants are adapted to bees or not.

By deploying a new camera-trapping method that I am developing to record insect visitation, I was able to gather several days of pollinator observations, despite some very bad weather. After initially being baffled as to what honeyeater might visit such a low ground-hugging shrub, I got my answer after day one, when I captured video of my new favourite bird: the Tawny-crowned Honeyeater (Gliciphila melanops) feeding on the flowers. Furthermore, the recordings of honeybee fly-bys are sufficient to rule them out as pollinators.

This little result is a win on two fronts: a successful trial of new pollinator-monitoring cameras, and vindication of predicting pollinators from flower morphology.

Click here for the full HD video.

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Photos from the field: East Gippsland, Victoria

I recently began a brand new project with the University of Melbourne. The beginning of a new project is filled with equal parts excitement and trepidation—excitement at the novelty, the blank canvas, the potential, and trepidation at not wanting to put a foot wrong in critical early decisions that will affect the outcome of a career-defining opportunity.

Here the photos from a first foray into East Gippsland, surveying sites for bird-pollinated Prostanthera walteri.

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Mt. Elizabeth

 

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Snowy River National Park

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Prostanthera walteri

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Prostanthera hirtula

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McKillops Bridge

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The Snowy River

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The Snowy River

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Prostanthera walteri

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Snowy River National Park

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Gippsland waratah – Telopea oreades

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Floral diversity in Prostanthera

 

As you were, Australian researchers.

Waking up to look at this before a coffee and a shower was enough to put me into fight or flight mode this morning.

With hackles raised I read on and found a sciency corner of Australian Twitter users in a flap about Abbott’s 20% ARC cuts. #AbbottsRazor #ARCcuts etc etc

While the wording of these Tweets is strictly true, they are also completely misrepresenting the politics of these ARC funding estimates.

The numbers are below. The top row is the current budget handed down by Labour in 2013. The middle row is the Abbott Government amendment. The bottom row is the difference. Numbers represented in thousands (000’s).

2013-14

2014-15

2015-16

2016-17

TOTAL

May budget

$883,959

$879,983

$834,587

$788,710

$3,387,239

Amendment

$883,959

$853,110

$783,253

$716,205

$3,236,527

Difference

$0

$26,873

$51,334

$72,505

$150,712

YES. ARC funding will dive by 19% in the next 4 years. But this is a dive courtesy of the Labour Government’s May 2013 budget.

YES. Abbott is cutting funding further, but this amounts to 4% cut in total ARC spending over the next 4 years. The majority of the sliding investment trend came from the initial budget trajectory set out in May.

The time to make a flap about budget cuts was in May. And some of us had a good whinge then. The truth of this latest news is that it is a continuation of the prevailing “death by a thousand cuts” trend, as another shaving is whittled off our future investment in research and innovation.

But the big lesson here is to hold fire when it comes to social media. A forgiving person might acknowledge that this shows that scientists are only human, prone to the occasional passionate, emotional, reactionary outbursts. A harder judge might question whether researchers who don’t think critically and do a bit of their own “research”, deserve any ARC funding at all.

Thanks Alice Hutchings, for engaging your brain. And Tom Stayner for the title.

Postscript

Jeremy Shearman from the Genome Institute in Thailand has produced this graphic showing the effect of amendments on ARC funding over the last few years. The trend is one of providing more upfront dollars with increasingly steep sliding scales of less funding later.

ARC funding amendment history