Occasionally in some species—mostly insects—we see the phenomenon of gynandromorphs: individuals that, through a genetic or developmental accident, have parts of the body that are male, and other parts that are female. They are patchworks of sex. These are most easily spotted in insects, but may have been missed in other species (alternatively, gynandromorph insects may be more viable than, say, gynandromorph mammals or birds, though I have posted on a gynandromorph cardinal). The various posts I’ve done on gynandromorphs are collected here.
Five years ago Matthew and I wrote a post about how gynandromorphs are formed, something well known genetically in our fruit flies (Drosophila). Using special genetic tools, we can also produce gynandromorphs at will. This involves a special X chromosome that gets lost easily during cell division. If you put one special X in females (XX), the tissues in which the X gets lost become XO, which happens to be male tissue, though XO males are sterile. The chromosome loss can happen at various stages of development, so you can get flies split straight down the middle (if the X gets lost at the first cell division), or flies with various-sized patches of male and female tissue.
Here are a few examples from flies (white bits are XO male parts and shaded are XX female parts). Note that the upper-left fly is split straight down the middle. I’ve seen a few of these in my time.
Finding gynandromorphs in nature is rarer, as wild insects are small, mobile, and not easily inspected. But the researchers on the paper below, published in The Science of Nature, found a gynandromorph jumping spider whose right half was male and left half was female. This is easily seen (given that the spiders are tiny: 4-6 mm, or 0.15-0.25 inches), for the spiders are sexually dimorphic, with the males having much larger fangs and chelicerae (mouthparts) than females, as well as different pedipalps (“palps”), distal segments of the legs that serve not only for sensory detection, but also for courtship display and sperm transfer in males.
Having a live spider whose right half is male and whose left half is female immediately gives you the chance to answer a question: “Does this weirdo spider behave as a male, as a female, or both?” This is the question that the researchers answered in the paper below.
You might be able to access the article by clicking on the screenshot, as it’s free with the legal UnPaywall app. The pdf is here and the full reference is at the bottom of this post. If you can’t get the pdf, make a judicious inquiry.
The jumping spider Myrmarachne formicaria is palearctic, and has been introduced in the U.S. The authors found one gynandromorph in Japan in October of 2016, as well as a bunch of normal males and females, which could be used to test the sexual/antagonistic behavior of the gynandromoprph. Here’s what it looked like (see caption below). The very large fangs and chelicerae can be seen on the spider’s right—the male side, as they’re much larger in males than in females. (We don’t know how this individual came about, though I suggest one way below.)
And the palps were also different on the two sides, for the male palps—the spider equivalent of a penis—differ from those of females. (a) shows the ventral view of the right palp in the gynandromorph, and (b) the ventral right palp of a normal male. As you see, the right palp is male, designed to hold sperm. The left palp of the gynandromorph (c) is identical to a normal female palp (d). Females receive sperm in the genital area (“epigyne”), put there by the male’s palps.
The genitals were also split down the middle, with the gynandromorph having a normal female epigyne (the female genital opening that receives sperm) on the left side (e), with a normal female shown in (f), while the right side of the gynandromorphs (arrow) is screwed up, as males don’t have epigynes.
So we have a spider split straight down the middle, from fore to aft. This may have involved the loss of a chromosome in an original female zygote, as normal female spiders are XX and males X0, lacking a Y chromosome. If an XX female zygote lost one X chromosome at the first cell division, one half of the spider would be female (XX) and the other half male (X0), and it could be split down the middle, as this one is. There are other explanations, but this seems the most likely.
So how did this gynandromorph behave—as a male or a female?
The results can be stated briefly: the spider behaved as a male and was perceived as a male by other males. In the (a) part below, you can see the behavior of normal males, who, when they recognize each other, bend their abdomens, move from side to side, open their legs and raise their chelicerae, and, occasionally, engage in battle, trying to topple each other with their chelicerae. (The numbers show the number of pairs in which different behaviors were seen; the one fight is at the bottom.)
(c) shows the gynandromorph male pitted against other males (four trials). The red spider is the gynandromorph; the black one a normal male. The same bending of the abdomen and moving from side to side (“pre-fighting behavior”) was seen in both spiders, indicating that the gynandromorph was not only perceived as a male, but itself behaved as a male. The arrow shows that all four antagonistic interactions terminated without a fight.
What about the gyandromorph faced with a female? Normal male-female courtship behavior is shown in (b). Males approach the female from the front, stretch their legs out to touch the female, and sometimes the female stretches out her legs, too. Neither of the two regular courtships resulted in a mating, which isn’t surprising. (Females are picky.)
Finally (d) shows the gynandromorph (red) encountering a female (black); there were two trials. The gynandromorph male approached the female and reached out his front legs to touch her, just like “normal” males. In these cases, though, the females ran away when this happened, so we don’t know if the females perceive the gynandromrph as male or as some kind of weirdo.
The paper also has videos of the mating and antagonistic behavior here.
The upshot: The gynandromorph, though morphologically half male and half female, behaves as a male, both in interactions with other males and with females. Further, it’s perceived as male by other males, while we don’t know how the female perceived its sex (she might even be confused). This shows that although morphology is split down the middle, behavior seems to be male-specific.
Why is this? We don’t know if the brain, presumably the seat of behavioral repertoires, is split down the middle, which might cause muddled behaviors. The inside of the spider might not show the same pattern as the outside. Alternatively, even though the brain might be half male and half female, the hormones and other chemicals that militate behavior might show male dominance, effacing any female behaviors. It’s interesting that the authors list seven other cases of gynandromorphs in spiders and insects, and in six of these the piecemeal individual behaved as male (the exception was a bee that didn’t show male-specific behavior towards a queen).
This experiment needs to be tried with Drosophila, and I don’t think it has been yet. For in flies we have far more sophisticated ways of changing very small parts of the fly from one sex to the other, and it would be better to use those methods than to use the relatively crude method of manipulating the parts of the fly visible only from the outside. With these techniques in flies, we could determine what parts of a fly must be male to show male behaviors, and what parts female to show female behaviors. That’s a really good question but, as Matthew said, “the cool kids aren’t interested in it.”
h/t: Tony
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Suzuki, Y., Kuramitsu, K. & Yokoi, T. 2019. Morphology and sex-specific behavior of a gynandromorphic Myrmarachne formicaria (Araneae: Salticidae) spider. Sci Nat 106, 34.. https://doi.org/10.1007/s00114-019-1625-x
Dumb question:
Is X inactivation active in the example here?
Anyone?
Fascinating. It will be interesting to learn answers to the two big questions – 1)is the internal morphology also split? and 2)are male hormones etc dominant?
Hi Janet,
I don’t know how it works in spiders, but fruit flies have no sex hormones. Each cell in the fly’s body decides for itself whether it is male or female, by counting its X chromosomes (more specifically, the ratio of its X chromosomes to autosomes). XX cell = female, X cell = male.
Very discerning, those damn flies. I find them drowning in my cider and wine and know how important their species is. I drink them and don’t care. My wife recoils, which doesn’t help because I chuckle. Why do we males like to disgust out female loved ones? No studies here. Thanks for another cool science post.
Uh oh, so in this case sex is a quantum binary??? just kidding.
Keith
Thanks for this interesting post. Kudos to the investigators who found the spider and realized that they could keep it alive and do these tests.
Very interesting science. I especially liked the assessment of how the spider itself behaves, which IMO is critical for understanding what’s going on; it would be easy enough to explain other male behavior as simply cueing off of the big fang, but that wouldn’t explain the spider’s own behavior.
“she might even be confused”
Probably so.
But could she be fertilized? First there is behavioral issues, then the plumbing issues.
This is a good question
Fascinating indeed. So the spider is not sterile? And procreates as a male, seeing as most of its behaviour was male-like? And the bee that didn’t show male-specific behaviour towards a queen – that doesn’t say that the bee showed female behaviour. Fascinating (again)! Surely some cool kid will pick up on this as a research project? Sounds like a good opportunity (and a good proposal with a strong story to write).
As for whether the female perceived the spider as another male, I think you need to offer control males to those particular females. Jumping spiders will reject perfectly normal males as well.
Perhaps there is neural wiring that crosse between the L and R sides of the brain (or ventral nerve ganglion which controls the legs) so the male side can direct gestures on the female side.
Thank you so much for this article. Totally captivating! (see, I didn’t repeat ‘fascinating’, the first word to come to my mind)
Also, a good starting point for a short story, let’s imagine a human instead of the insects.
Many thanks as ever for an amazing bit of science.
Very, very good. I had forgotten about gynandromorphs. One wonders what personal pronouns these insects choose for themselves. But of course—they could choose all four, and nobody could say nay to that.
I don’t know about jumping spiders but I’m pretty sure that ants prefer to be called THEM!
My apologies to any youths whose childhoods have thus far been bereft of beautifully cheesy black and white sci-fi movies and as a consequence cannot fathom the meaning of my post.
And even beyond the American ones, C., we have the ineffable Japanese branch of the franchise. Can anyone forget Gojira!, and his/her/its junior Ritorugojira? Not to mention Mothra, Rodan, and Ebirah (the monster prawn)!
Absolutely fascinating. A continuum between male and female.
sub
Perhaps the “cool kids” aren’t interested in studying this because the spider showed male dominance. Or maybe I’m just being cynical. One would think that gynandromorphy would be obsessively studied by the new “sci-deologues” who seem to be pushing politics into science to support their pre-determined anti-biological sex beliefs. Again, I’m being cynical so ignore that but I do find it fascinating. I’m sure there’s at least a book’s worth of philosophical pondering in this anyway. It appears that in nature, like the navy, anything that can go wrong will go wrong and what interesting things there are to learn about such cases.
When I was a grad student, I sorted through thousands of Drosophila, and one day I found a classic gynandromorph, split right down the middle! Its external genitalia were half female, half male. I saved it in a separate vial, hoping to mate it with males and with females in series, to see what would happen – would it be capable of mating and producing progeny with each, either one, or neither? For example, would it be capable of inseminating females with its half-formed clasper? Sadly, the gynandromorph expired before I had the chance to test it. Still, it was really cool to observe it – put a nerdy smile on my face.
Thanks for putting the time into writing this. I know you don’t get as much feedback on these posts as you do on posts regarding topical issues, but it’s information like this that feeds a sense of wonder, amazement and curiosity about the world. It’s a kind of nourishment you don’t get from politics!
Like Johnny Cash’s boy named Sue, ya gotta be tough to survive with that mixed up morphology.