Does a split jumping spider, half male and half female, behave as a male, a female, or both?

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.)

(From paper): External morphology of a Myrmarachne formicaria gynandromorph (a–d) and normal individuals (e, f). a Dorsal view; b ventral view; c enlarged dorsal view of gynandromorphic chelicera; d enlarged ventral view of gynandromorphic chelicera; e enlarged ventral view of normal male chelicera; f enlarged ventral view of normal female chelicera. Scale, 2 mm (a, b); 0.5 mm (c–f)

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.

(From paper): Sexual organs of the gynandromorph (a, c, e) and normal individuals (b, d, f). a, b Ventral view of the right palp; c, d ventral view of the left palp; e, f epigyne. The white arrow indicates the spermatheca at an abnormal position. Scale, 0.1 mm

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.

(From paper): Flow diagrams of the behavioral sequences of agonistic behavior (a, c) and courtship behavior (b, d) performed by non-gynandromorphic individuals (a, b) and among gynandromorphic and normal individuals (c, d). Abbreviations: g, gynandromorph. Numbers within parentheses indicate the observed number of individuals that showed the behavioral elements per total number of observations

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

________________

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

23 Comments

  1. ThyroidPlanet
    Posted September 25, 2020 at 9:41 am | Permalink

    Dumb question:

    Is X inactivation active in the example here?

    • ThyroidPlanet
      Posted September 25, 2020 at 2:11 pm | Permalink

      Anyone?

  2. Janet
    Posted September 25, 2020 at 9:51 am | Permalink

    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?

    • drosophilist
      Posted September 25, 2020 at 3:40 pm | Permalink

      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.

      • Mark R.
        Posted September 25, 2020 at 10:26 pm | Permalink

        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.

  3. Keith
    Posted September 25, 2020 at 10:17 am | Permalink

    Uh oh, so in this case sex is a quantum binary??? just kidding.

    Keith

  4. Posted September 25, 2020 at 10:27 am | Permalink

    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.

  5. eric
    Posted September 25, 2020 at 11:51 am | Permalink

    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.

  6. rickflick
    Posted September 25, 2020 at 11:53 am | Permalink

    “she might even be confused”
    Probably so.
    But could she be fertilized? First there is behavioral issues, then the plumbing issues.

    • EdwardM
      Posted September 25, 2020 at 1:36 pm | Permalink

      This is a good question

  7. sgo
    Posted September 25, 2020 at 12:16 pm | Permalink

    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).

  8. Posted September 25, 2020 at 1:10 pm | Permalink

    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.

  9. Alicia
    Posted September 25, 2020 at 1:12 pm | Permalink

    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.

  10. Steve Pollard
    Posted September 25, 2020 at 1:12 pm | Permalink

    Many thanks as ever for an amazing bit of science.

  11. Jon Gallant
    Posted September 25, 2020 at 1:21 pm | Permalink

    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.

    • C.
      Posted September 25, 2020 at 2:32 pm | Permalink

      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.

      • Jon Gallant
        Posted September 25, 2020 at 4:34 pm | Permalink

        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)!

  12. Posted September 25, 2020 at 1:35 pm | Permalink

    Absolutely fascinating. A continuum between male and female.

  13. Ken Kukec
    Posted September 25, 2020 at 2:14 pm | Permalink

    sub

  14. C.
    Posted September 25, 2020 at 2:52 pm | Permalink

    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.

  15. drosophilist
    Posted September 25, 2020 at 3:45 pm | Permalink

    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.

  16. Rik G
    Posted September 25, 2020 at 7:44 pm | Permalink

    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!

  17. Posted September 25, 2020 at 7:58 pm | Permalink

    Like Johnny Cash’s boy named Sue, ya gotta be tough to survive with that mixed up morphology.


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