pictures in my head: What is that on the wing of the fly? What does it tell us about adaptation?

Over the past week or so, there has been an absolutely amazing image that has made the rounds on the internet of a fly (Goniurellia tridens)with markings on its wings reminiscent to many viewers of ants. 

Goniurellia tridens is a 3-in-1 insect [photo: Peter Roosenschoon] pic.twitter.com/i8ThAOkrvN
— Ziya Tong (@ziyatong) November 4, 2013

As described in these blog posts and articles (Anna Zacharias, Jerry Coyne, Morgan Jackson, Andrew Revkin, Joe Hanson, also here and here) about it, the assumption is that these images are used by this fly to mimic the ant (or more likely a spider- more on this below), to act to ward off potential predators. However, there has been relatively little discussion about the context in which it uses it (but see Morgan Jackson's post), and demonstration of its adaptive utility. As pointed out by many evolutionary biologists, and discussed in detail by Gould and Lewontin in one of the most famous papers in evolutionary biology (The Spandrels of San Marco and the Panglossian paradigm: A critique of the Adaptationist programme), it is easy to make a "just so" adaptive story, but as scientists we need to perform critical experiments demonstrating the adaptive utility of this picture on the wing.

As numerous commenters on the blogs and on twitter have pointed out this fly is part of the family of true fruit flies (Tephritidae), that include several that are known to startle jumping spider (causing them to do a short retreat). This retreat is likely because the flies have evolved to mimic aggressive behaviours of the spiders themselves. This work was initially described over 25 years ago in a pair of papers in Science (One by Erik Greene, Larry Orsak and Douglas Whitman. The other paper by Monica Mather and  Bernard Roitberg). These papers beautifully demonstrate the adaptive utility of markings on the wing combined with a rowing action of the wings that could achieve this mimicry. Neither the markings on the wings nor the rowing behaviour alone were sufficient to induce the aversion behaviour in the spiders (the spiders retreat). Indeed those of us who took biology courses in University in the early to mid 1990's probably remember this example being taught to us. What's more is that it seems to be fairly wide spread among species in this family of flies (each research group used a different species of Tephritid fly and spider.) Another paper (Oren Hasson 1995) tested about 18 different species of jumping spiders with the medfly (also a Tephritid), and showed that most spiders responded with the retreat as well. This suggests that this adaptive wing morphology and behaviour combination is probably pretty ancient.

Here I want to show you a video of a picture-winged fly, with a jumping spider. This fly is from a totally different family of flies (the picture-winged flies Ulidiidae (formerly Otitidae)) than the ones discussed above (Tephritids), but apparently does the same thing to startle jumping spiders (as a way of escaping being eaten) as the true fruit flies. 

 A few years ago, when I was hosting a lab bbq in my backyard, we were lucky enough to get to watch the intricate little behavioural "routine" between a fly and a jumping spider (in this case the bold jumping spider, Phiddipus audax). The spider approached the fly, got into its attack posture, and then the fly did its "wing rowing" display, the spider "retreated" (took a short jump back), and the fly took off, successfully evading getting eaten. Not too shabby, plus how often do you get to watch this for real!

Two years ago I got to watch this happen again, and this time I happened to have some collecting vials. So I collected the flies! I then put the fly in a small dish with a jumping spider  (the zebra spider Salticus scenicus) so I could get some simple video of it. Here it is in all its grainy, low quality glory.

Given that I am not a great entomologist, I sent a picture of the fly off to a colleague (Jim Parsons, our collection manager in the MSU Entomology department), and he pointed out to me that this was not a true fruit fly (Tephritid) at all, but a picture-winged fly (from the family Ulidiidae). This particular fly is called Delphinia picta.

This was clearly really exciting, as it shows the potential for a whole other group of flies demonstrating a similar set of anti-predation behaviours. While both of these families belong to the same super-family, their last common ancestor lived probably 75 million years ago (give or take several million years).  Is this an example of two different groups of animals independently adapting the same way (convergence) to a similar selective pressure (not getting eaten)? Or is it an adaptation that has survived for millions of years across many species? Finally the possibility exists that some aspects of the behaviours and wing spots allow this to evolve as an anti-predator adaptation over and over again (parallelism)? Whatever it is, it suggests that something even deeper and cooler has happened in evolution, and it will be great to figure this out (hint to new graduate students seeking projects!). As my colleague Rich Lenski mentioned to me (when I showed him this video), it also makes one think carefully about the appropriate "null hypothesis" regarding putative adaptations!

  In my lab, one of the things we study is the fly Drosophila melanogaster, and how it evolves in response to potential predators, including jumping spiders. Drosophila is the little fly that you used in high school or university biology.  Many call it a fruit fly, even though it isn't (pomace fly and vinegar fly are both used as its common names). For Drosophila we have never observed this kind of behaviours at all. However Drosophila does display a pretty wide range of behaviours, and we are writing up a paper about it right now. For a taste of some of it, check out my graduate students poster over on figshare describing some of the behaviours. 

Let me know if you want more, and maybe I can post some additional video. However, to whet your appetite here is another related video that we posted a while ago to youtube (of flies with a mantid). The action starts at about 2:30 into the video.

Our new pre-print: An integrative genomic approach illuminates the causes and consequences of genetic background effects

This is a guest post by Dr. Chris Chandler. Cross posted from Haldane's Sieve.

Biologists have long recognized that a mutation can have variable effects on an organism's phenotype; even introductory genetics classes often make this observation by introducing the concepts of penetrance and expressivity. More mysterious, however, are the factors that influence the phenotypic expression of a mutation or allele. We know, for instance, that introducing the same mutation into two different but otherwise wild-type genetic backgrounds can result in vastly different phenotypes. But what specific differences between these two genetic backgrounds interact with the mutation, and how? And how does gene expression fit into this puzzle? Answering these questions has not been an easy task, which is not too surprising when you realize that penetrance and expressivity are, in reality, complex quantitative traits. We therefore adopted a multi-pronged genetic and genomic approach to tease apart the mechanisms mediating background dependence in a mutation affecting wing development in the fly Drosophila melanogaster.

The phenotypic patterns seen in our model trait have already been characterized: the scalloped[E3] (sd[E3]) mutation has strong effects in the Oregon-R (ORE) background, resulting in a tiny, underdeveloped wing, while its effects in the Samarkand (SAM) background are still obvious but much less extreme, resulting in a blade-like wing.

To try to find out what causes these differences, we generated and combined a variety of datasets: whole-genome re-sequencing of the parental strains and a panel of introgression lines to map the background modifiers of the sd[E3] phenotype; transcription profiling (using two microarray datasets and one RNA-seq-like dataset), including analyses of allele-specific expression in flies carrying a "hybrid" genetic background; predictions of binding sites for the SD protein, which is a transcription factor; and a screen for deletion alleles that enhance or suppress the sd[E3] phenotype in a background-dependent fashion.

Our results point to a complex genetic basis for this background dependence. We found evidence for a number of loci that are likely to modulate the effects of the sd[E3] allele. However, some unexpected inconsistencies provide a cautionary tale for those intending to take a similar mapping-by-introgression approach for their trait of interest: do multiple replicates, and introgress in both directions, or you may inadvertently end up mapping some other trait! Although the number of candidate genes we identified were generally large, by combining those results with data from our other datasets, we were able to narrow our focus to those showing a consistent signal, yielding a robust set of candidate genes for further study. Without getting into too much detail, we also used a novel approach to show that background-dependent modifier deletions of the sd[E3] phenotype (of which there are many) involve higher-order epistatic interactions between the sd[E3] mutation, the deletion, and the genetic background, rather than quantitative non-complementation (so more than two genes were involved).

Overall, we think that an integrative approach like this could be useful for others trying to understand complex traits, including genetic background-dependence of mutations. In addition, if you're a Drosophila researcher working with the commonly used Samarkand or Oregon-R strains, our genome re-sequencing data (raw and assembled), including SNPs, will soon be available in public repositories for genetic data.

Go to the pre-print of the paper on arXiV.

A new manuscript on experimental tests for genetic constraints from the lab

Just a quick note, we have posted an updated manuscript (submitted to Evolution) to arXiv. I will post more about it soon (and hope to have it linked to Haldane's Sieve). In any case, while it has taken a really long time to get the analysis and interpretation quite right, I think it is a nice example of merging developmental genetic and evolutionary quantitative genetic insights!

Three cheers for the little guy....

Now, I have something to admit. Some of you may be shocked and dismayed, and perhaps even amazed by my admonition. I work with fruit-flies, and it makes me very happy.... More than that I have to say I even love these little critters.

There, I said it.... I have come clean.


Of course when I say I work with fruit flies, what I mean to say is I work with that particular little guy which is sometimes called the vinegar fly, pomace fly, or with its scientific name, Drosophila melanogaster which loosely translates to "black bellied dew lover". Yes, I mean that dreaded fly who you had to work with in high school biology, and may still haunt you when you fail to rinse out old wine or beer bottles. That little fly.


Why on earth would I say I love these little guys? Am I just one more really strange scientist? Well, I like to think that while I may be a bit quirky, I am not quite that much of an oddball. The truth is, that the love I feel for these little fruit flies is not that of a spouse, or parent or child, but the love of something whose very nature can transform the way that we think of the world.

Oh, so very hokey, I know. However, over the past decade or so that I have worked with Drosophila, I have been truly amazed by the insights we can gain from little more than a small microscope, some mushy bananas and a paint brush. Now this may surprise some people, but I consider myself a little bit of a Luddite. Clearly I can use a computer, well enough, and I even know how to set my DVR (but apparently so does my 3 and half year old...), but when it comes to the rapid changes that are happening in methodologies and technologies in the biological sciences, I have to admit I am a bit of a slowpoke.


Yet, many of the most amazing discoveries made using fruit-flies have been done using basically the same technology as was used in the early 20th century when these first became a "model" for studies in genetics. Basically we play match maker for the fruitflies, and then wait to see what happens. Are their offspring normal, do they have wacky abnormalities? We then go about figuring out what these wacky abnormalities do, and how they are caused.

Ok, so I am oversimplifying. There is a lot more than that. However, what is true is that it is people doing the work (us mad scientists to the rest of y'all) that spend lots of time thinking about how best to do the match-making (what we call genetic crosses). Indeed over a decade ago the Nobel prize was won by three fly geneticists who thought carefully about how to study early development of an organism, how best to set up these crosses and look for abnormalities. The work that they did with not much more than the flies, and some microscopes laid the foundation for almost everything we know about the genetic basis of early development, including in humans.

So as long as you are observant and reasonably patient, you too can be a fruit-fly geneticist!!!

These approaches were then fine tuned to discover literally thousands of other genes, and in particular the use of what are called sensitization screens have found many genes that we now know can contribute to various aspects of human cancers. Pretty impressive work for a little fruit-fly.

Now with the amazing technological and methodological breakthroughs some scientists suggest we are entering the "post-genomic era". What this means is that as it has become much less expensive to find out all letters and words (the genes) of DNA in an organism. These fragments of DNA that are sequenced (our words) can be fed into super-computers (using some very cool computer programs) to reconstruct these words into the sentences, paragraphs, chapters and ultimately the book that is the "genome" of any animal, plant or microbe we want.

Given these breakthroughs, there have been some suggestions that the original model organisms (like the fruit-fly) will become less useful, despite all of the tools and data that has been gathered. That is we will be find out many of the same things in other species, that are perhaps nearer and dearer to our hearts, or at least are nicer to look at. Yet, I do not think the time of the fly has passed. I suspect that Drosophila will continue to claim the hearts of a new generation of scientists, and I imagine that it still has a trick or two to teach us all!