"We propose a shift from asking ‘Why engage in same-sex sexual behavior'
November 18, 2019 12:44 PM   Subscribe

... to 'why not?' " Julia Monk writes about queering evolutionary theory for the Nature Ecology and Evolution research community. A new review in Nature Ecology and Evolution, An alternative hypothesis for the evolution of same-sex sexual behaviour in animals, identifies the heterosexist biases that underpin decades of investigation in the evolution of sexual behavior. Most tellingly, most scientific investigations that seek to explain how same-sex sexual behavior (SSB) may evolve and persist in a population of animals start from the premise that different-sex sexual behavior was the ancestral position.

The authors, including MeFi's own sciatrix, to the thunderous boom of forehead smacking across biology departments worldwide, suggest that a better null hypothesis for sex is "indiscriminate sexual behavior":
"We reason that the perfectly targeted DSB [different-sex sexual behavior] assumed in current models are more likely a derived trait that arose after the evolution of sexual behaviours in an ancestral anisogamous, multicellular, immobile species." (In other words, sex evolved before sexual dimorphism, duh.)
The full paper is pay-walled because Springer, but I bet there's probably someone who has their Author's Accepted Manuscript if you find yourself really in need of the deep dive and need to ask. Title for this post taken from co-author Ambika Kamath's twitter feed.

Previous queer animals on Metafilter: Birds, all animals, penguins, possibly sheep.
posted by Made of Star Stuff (47 comments total) 88 users marked this as a favorite


 
The paper is actually available on Research Gate here.
posted by Made of Star Stuff at 12:46 PM on November 18, 2019 [8 favorites]


Woo-hoo Nature paper sciatrix! Congratulations!
posted by Frowner at 12:55 PM on November 18, 2019 [46 favorites]


How biologically exuberant!
posted by mittens at 1:23 PM on November 18, 2019 [4 favorites]


This sounds fascinating. Though a non-expert, I'd like to read more - so does anybody know if there are any good public forums where I could go and look for sensible scientific-minded reaction to this paper and discussion of its approach and implications?
posted by vincebowdren at 1:49 PM on November 18, 2019 [1 favorite]


I want to know how this handles fungal mating types. (Which aren't sexes in the mammalian—or even flowering plant—sense, but make my brain melt whenever I contemplate them because biological exuberance is all very well but who needs 300 sexual-assortative traits?)
posted by cstross at 1:52 PM on November 18, 2019 [4 favorites]


Half of me wants vincebowdren’s “sensible scientific-minded reaction to this paper and discussion of its approach and implications.”

The other half wants to go to a dolphin circuit party with my two buddies (one’s a poly albatross, the other’s a bag of gay spiders) and shout enthusiastic comments about this paper over thumping house music til we give up and just dance it out.
posted by sixswitch at 2:00 PM on November 18, 2019 [19 favorites]


but who needs 300 sexual-assortative traits

my friday night was looking kinda empty


PS: sciatrix, congrats!
posted by lalochezia at 2:00 PM on November 18, 2019 [9 favorites]


I'm very excited to read this - congratulations Sciatrix et al!
posted by ChuraChura at 2:24 PM on November 18, 2019 [3 favorites]


a dolphin circuit party with my two buddies (one’s a poly albatross, the other’s a bag of gay spiders)

The classic-era B-52’s missed a song opportunity, I think. (“Hi! I’m Kate! And I’m a poly albatross!” etc.)

This is wonderful and I like it. “Biologically exuberant,” indeed. Go Sciatrix!
posted by mykescipark at 3:10 PM on November 18, 2019 [1 favorite]


This is awesome. Thank you.
posted by PMdixon at 3:26 PM on November 18, 2019 [1 favorite]


i don't feel like i understand what this means but i'm just imagining the fun and productivity of getting to work with other lgbt professionals creating an environment like this:

There were times when we disagreed, but always respectfully and with curiosity about each others’ perspectives. This friendly and undefensive disagreement helped fine-tune the clarity of our arguments.

and then the fear of bringing it into the larger world and going from a collaborative space to a potentially combative one. i'm so glad this kind of work is being done! congrats sciatrix!!
posted by gaybobbie at 3:40 PM on November 18, 2019 [8 favorites]


THe paper was fascinating and seems to rock solid from this complete non-expert's perspective. That last sentence linking the search fpr social justice and equity with the search for scientific discovery was downright inspirational. It's so great to see these arguments being made within science and in the language that science expects and respects, and that consulting with eg the Queer Ecologies group at Berkeley (which itself sounds awesome) seems to have been generative.

And I echo the congratulations to sciatrix! I hope this gets the fair reading and debate it deserves, and that a more productive research paradigm follows. (My own attempt at an inspirational closing sentence has fallen a little flat.)
posted by col_pogo at 4:01 PM on November 18, 2019 [3 favorites]


congrats, sciatrix!
posted by kokaku at 4:01 PM on November 18, 2019 [2 favorites]


I'm still just kind of reeling from reading the paper and thinking "Jesus, why did I just accept the idea that same-sex sexual behavior was derived from different-sex sexual behavior?" My favorite little example from the paper: "For example, male burying beetles engage in more SSB when the perceived costs of missed mating opportunities with females were higher, suggesting that exclusive DSB could be disadvantageous when mating opportunities were rare." At first blush, that seems a little odd, since why would it be advantageous to try to mate with the same sex (right because you can't make babies with them so it wouldn't increase your fitness?) -- but the whole point is that if you're being too picky, and mating opportunities are rare, you might miss a compatible mate. "You miss 100% of the shots you don't take" says the male burying beetle, furiously attempting to copulate with another male burying beetle.

It's a really good paper. It probably will be read in a lot of behavioral ecology seminars in the following months. It has some really neat implications for the evolution of sexual dimorphism, which we might now think would be more likely to evolve if the costs of SSB are higher on average; and could be a way to explain secondary loss of dimorphism. I'm still trying to sort out if this might change the approaches to sex-specific mimicry in swallowtail butterflies.
posted by Made of Star Stuff at 4:27 PM on November 18, 2019 [12 favorites]


Way to go, sciatrix!! *high-five*

This just—yes, of COURSE! Bless you all for putting your finger on the inherent wrongness of the prevailing heterosexist explanation and sweeping it away! So many exclamation points!!
posted by epj at 4:35 PM on November 18, 2019 [2 favorites]


Holy shit this is DOPE.

Congrats, sciatrix!!
posted by schadenfrau at 4:44 PM on November 18, 2019 [1 favorite]


*grin* Thanks, everyone! We're collectively beyond excited and pleased with the reception the paper has gotten, and have been showing each other responses and chattering at one another all day. It's been purely lovely, and we fully intend to keep working with one another as we progress through our careers. (Caitlin, Julia and I are still in our PhDs; Ambika and Max are postdocs. So we're all very early career.)

This sounds fascinating. Though a non-expert, I'd like to read more - so does anybody know if there are any good public forums where I could go and look for sensible scientific-minded reaction to this paper and discussion of its approach and implications?

If you'd like to ask questions, I'll be around. If you just want to read more on the topic, I can recommend a few other papers and books, too? I actually do not know of a place which is better than MeFi or Biology Twitter to host that kind of discussion, but I also freely acknowledge that me sitting in the room in both places makes things a little tricky for open critique.

I want to know how this handles fungal mating types. (Which aren't sexes in the mammalian—or even flowering plant—sense, but make my brain melt whenever I contemplate them because biological exuberance is all very well but who needs 300 sexual-assortative traits?)

Oh, that's an awesome question. We made a conscious choice to focus on sex after the evolution of anisogamy, which is to say eggs and sperm, mostly because fungal mating types are their own vein of complicated and none of us has a ton of experience with them but also because we were focused broadly on behaviors relating to sex-the-activity rather the evolution of sex-as-in-eggs-and-sperm. That being said, as I understand them, fungal mating types aren't quite an anything-goes as far as reproduction goes: for species with more than two, not all mating types are actually reproductively compatible with all other types. Now, the line between sexual behavior and fertilization is blurrier than you might think, but I don't think that there's much in the way of fungal behavior to attempt to avoid mixing gametes that aren't reproductively compatible and only allow the reproductively compatible gametes to touch. Does that make sense?

We actually do talk about SSB in species who organize sex differently, though. For example, one of the species we put into Fig. 1 is the bluestreak wrasse. These guys start life as female and transition to male based on certain social and size-based cues; however, females who will become male will actually start spawning with other females and taking male courtship roles before their gonadal transition starts at all. I think C. elegans was on my list of species to include before I opted to leave them out of the table because I wanted to focus only on species with reported SSB in wild contexts, but you do see these behaviors in contexts with more interesting ways of partitioning sex and reproduction as well.
posted by sciatrix at 5:14 PM on November 18, 2019 [49 favorites]


i don't feel like i understand what this means but i'm just imagining the fun and productivity of getting to work with other lgbt professionals creating an environment like this:

It's so good oh my god. I have gotten so much good shit out of working on this project and it's been such a lovely, supportive environment, and the Queer Ecologies group at UC Berkeley has been just totally amazing as well. *chinsquish*

It has some really neat implications for the evolution of sexual dimorphism, which we might now think would be more likely to evolve if the costs of SSB are higher on average; and could be a way to explain secondary loss of dimorphism.

Huh! I was certainly thinking mostly in terms of preference and the evolution of choice rather than dimorphism while writing it, but that's partly my bias: I work on trade-offs and changes in investment in social signals, so I'm primed to think in those terms. Now I'm thinking about ways in which sexual dimorphism might be expanding into different sensory modalities, not just the ones humans perceive most easily. Is sexual dimorphism just about signaling sex to other animals in your species, or is it a byproduct of other constraints in the species' social environment (e.g. size dimorphism as a function of intra-sex competition or reproductive investment needs), or is it some mixture of the two?

We've collectively been thinking a lot about costs while writing this paper, and wondering whether folks haven't been over-weighting the costs of sex and gamete production and under-weighting the costs of missed opportunities when studying these behaviors. I think that's one of the most important insights in this piece, speaking just for me.
posted by sciatrix at 5:25 PM on November 18, 2019 [24 favorites]


Congratulations, sciatrix! Nature! I can’t wait to read it and describe your hypothesis in conversation as often as possible!
posted by Knowyournuts at 5:27 PM on November 18, 2019 [2 favorites]


OH MY FREAKING HAPPY GODDESS

Sciatrix, I am in astounded joyful awe of you right now.
posted by nikaspark at 6:46 PM on November 18, 2019 [3 favorites]


Awesome! Can't wait to read this. Congrats!
posted by It's Raining Florence Henderson at 7:28 PM on November 18, 2019 [1 favorite]


wondering whether folks haven't been over-weighting the costs of sex and gamete production and under-weighting the costs of missed opportunities

This is really interesting stuff. Congratulations!
posted by Dip Flash at 8:33 PM on November 18, 2019 [2 favorites]


Do hermit species with rare social contacts have more SSB on average? If you're not mating continuously the cost of sperm or egg production may not be that high. The benefits from reduced parasitism in hermit species could offset the mate choice penalties.
posted by benzenedream at 11:33 PM on November 18, 2019


Man, the psychological swoop of reading about this paper in my different forums has been a rollercoaster.

Here: “Now I'm thinking about ways in which sexual dimorphism might be expanding into different sensory modalities, not just the ones humans perceive most easily.”

Over on Mastodon: “Good news everyone, the following list of animals are extremely gay.”
posted by mhoye at 11:36 PM on November 18, 2019 [10 favorites]


Forehead-smacking, indeed! Excelsior.
posted by eustatic at 12:22 AM on November 19, 2019 [1 favorite]


Wow! I love learning things that utterly demolish a previous perspective due to their simplicity and ability to explain things that had been ‘interesting anomalies’. Congratulations for introducing a true paradigm shift. I hope this will be required reading for any ethology or evolution class over the next ten years until it makes it into the textbooks.
posted by Emmy Noether at 6:01 AM on November 19, 2019 [3 favorites]


It does make sense that correctly identifying a mate of the appropriate gender had to evolve from ... not doing that. However, I am a bit amazed that everyone is viewing this is some big political triumph over The Man. It is a cool scientific insight, though. One of those “well, dud,” kinds of things where you think that if you had just been a bit smarter, you’d have thought of it yourself. Of course, you didn’t. Congrats on the paper.
posted by Gilgamesh's Chauffeur at 6:56 AM on November 19, 2019


However, I am a bit amazed that everyone is viewing this is some big political triumph over The Man.

It took queer scientists to suggest that different sex behavior might not have evolved first, that in fact same sex behavior might be ancestral, just as it took primatologists who were women to suggest that some assumptions about behavior in primates following human stereotypes might be wrong.

Sometimes The Man is wrong, and peoples long silenced have to be allowed in the lab and in the field to do the work and write the papers before we find out. The Man doesn't question his own assumptions about how the world works because he is invested in preserving his privilege.

(Congrats, sciatrix!)
posted by hydropsyche at 8:39 AM on November 19, 2019 [19 favorites]


I'm having some trouble understanding this, can someone break this down into a very simple timeline of what is being proposed?
posted by FirstMateKate at 9:59 AM on November 19, 2019


I'm having some trouble understanding this, can someone break this down into a very simple timeline of what is being proposed?

My very lay understanding is: homosexual behavior has always been assumed to be a thing that branched off from heterosexual behavior, because het behavior is the kind that makes babies and so obviously is more adaptive. Except, if you take a step back and look at the whole history of sexual behavior, it began with non-sexually differentiated organisms having sex with each other - in essence, homosexual behavior. Heterosexual behavior must have evolved from that, rather than the reverse.
posted by showbiz_liz at 10:09 AM on November 19, 2019 [3 favorites]


The basic idea is that - evolutionary biologists have thought same-sex sexual behavior was a weird anomaly that had to be explained, because the costs of engaging in sex without any reproductive benefit are very high. And the evolution of these behaviors has to be explained in every single species independently.

What these authors are proposing is that the common ancestor of all animals didn't have easy markers differentiating sexes, so they engaged in sexual behavior with everyone, regardless of sex, because the cost of a missed opportunity to successfully reproduce was too high. So a propensity for same sex sexual behavior is actually an ancestral condition for all animals, and it's only in relatively recent evolutionary time that different-sex sexual behavior (and obvious sex differentiation) has evolved.
posted by ChuraChura at 10:10 AM on November 19, 2019 [15 favorites]


Do hermit species with rare social contacts have more SSB on average? If you're not mating continuously the cost of sperm or egg production may not be that high. The benefits from reduced parasitism in hermit species could offset the mate choice penalties.

So the short answer is that we don't know. This gets me back to a point I've been meaning to make here and haven't, exactly: there is no systematic evaluation of species for prevalence of SSB or absence, and the literature is incredibly sparse. Often, presence of SSB only appears because someone bothered to write up a natural history note somewhere of a single incident they'd observed. This makes it really hard to do things like construct phylogenies of the evolution of SSB or ask empirical questions about its evolution on a macro scale or even ask questions about prevalence, because the groundwork just doesn't exist to answer those questions. Not yet, anyway.

That brings me to a point I'd like to make to bounce off what hydropsyche said: this work didn't appear out of thin air. It's been built heavily in particular on other works, largely (but not entirely) by LGBTQ scholars, trying to document SSB and provide discussion of it in nature. Back in 1999, Bruce Bagemihl said "Hang on, no one is looking at SSB in animals, but it seems to me that it's a lot more common than anyone thinks," and he wrote a book called Biological Exuberance: Animal Homosexuality and Natural Diversity documenting all the species he could find anywhere in the scientific literature, among other things. In that book, one of the things he really stresses is that no one is looking for these behaviors, and that when they are presented, they are often dismissed as not really sexual or otherwise minimized. Additionally, no one uses the same terminology, so it's hard to find these examples via literature searches.

Ten years later, in 2009, Marlene Zuk and Nathan Bailey wrote another article synthesizing work on the subject, explaining the various hypotheses that biologists had been using for the topic, and creating a short reference piece for evolutionary biologists to use when thinking about SSB. I put together most of Fig 1 and Table 1--originally intended for our joint poster this past summer, before they made it into the final piece--and I used both of those extensively as I was looking for examples. Paul Vasey, Malin Ah-King, Joan Roughgarden, and many others have also provided a ton of scholarship and resources that make a work like this possible, and many other folks are taking critical looks at animal sexuality that incorporate observations like this one. It's not just one exceptional person or group of people; it's scholarship that builds on the efforts of many people all working to understand the natural world that makes pieces like this work.

All of that being said, though: this is a really simple idea. It was honestly rather astonishing when we were first batting around the idea of this piece that no one had published it yet, and the reviewing process was an interesting mixture of "well, of course, this is obvious--why are you presenting it as if it's new?" and "that can't be right, SSB is costly with no obvious benefits!" (alongside a few people who went "well, this is obvious... well, hang on, I hadn't thought of that--what about this?). I don't think we've revolutionized science by publishing this idea, although I hope it will make biologists think a little bit more deeply about sexual behaviors.

I would like to update Dr. Bagemihl's book, twenty years on, or work on some kind of database to help aggregate this information and make it easy for biologists to report systematic appearances of SSB in their own systems. I definitely don't have time to do it myself right now--I need to graduate with my mostly-unrelated thesis, thanks--but it's a work that I would love to see done and/or help with, because that work would be an additional foundation to help new scholars tackle their own ideas.
posted by sciatrix at 10:36 AM on November 19, 2019 [15 favorites]


This is really interesting.

Is the idea that there were behaviors not related to sexual reproduction that were both same- and different-sex behaviors that were then co-opted by evolution to be used for reproduction? And that a behavior could be selected for because it led at the population level to increased sexual reproduction even though at an individual
level it wasn't necessarily a DSB.

That makes me wonder then at what point a behavior becomes a "sexual" behavior. Or maybe that trying to draw strict lines for that is a mistake? I really liked this part of the conclusion:
The notion that SSB is a recently evolved and distinct phenomenon from 'heterosexual' sex, rather than one component of the messy and tangled spectrum of behaviors, traits and strategies we clumsily refer to as 'sex' and 'sexual behavior' is symptomatic of the kinds of binary existentialism that hinder not only social liberation and equity, but also scientific discovery.
Like maybe we need to consider sexual behavior as a subset of some larger category of behavior?

Part of the problem maybe is teleological? I found myself thinking of some of the examples of SSB, like the burrowing beetle mentioned above, as "actually" a failed attempt at DSB. Like it's trying to mate with a female but accidentally mates with a male. But of course it's a mistake to think of the beetle as "trying" to so something. It just has behavior. And how closely related to reproduction does that behavior have to be before we think of it as a sexual behavior?
posted by straight at 10:44 AM on November 19, 2019


Thank you for explaining this! this is.. this just makes so much more sense?? that sexual dimorphism came after the development of sexual reproduction, as an adaptive evolutionary advantage. Right, that's what we're saying?
posted by FirstMateKate at 10:45 AM on November 19, 2019


The Man doesn't question his own assumptions about how the world works because he is invested in preserving his privilege.

Even when he's not - there are plenty of men who would like a more equal, more inclusive world - it's hard to question your assumptions when they seem to provide a complete and accurate worldview.

It takes people saying, "Hey, where the hell am I in this picture?" to notice the gaps.
posted by ErisLordFreedom at 11:10 AM on November 19, 2019 [9 favorites]


I am a bit amazed that everyone is viewing this is some big political triumph over The Man

Then I suggest you read up on the history of biological research into same sex behaviors.
posted by PMdixon at 12:21 PM on November 19, 2019 [7 favorites]


What these authors are proposing is that the common ancestor of all animals didn't have easy markers differentiating sexes, so they engaged in sexual behavior with everyone, regardless of sex, because the cost of a missed opportunity to successfully reproduce was too high. So a propensity for same sex sexual behavior is actually an ancestral condition for all animals, and it's only in relatively recent evolutionary time that different-sex sexual behavior (and obvious sex differentiation) has evolved.

TL;DR

MUST

FUCK

EVERYBODDDYYYYYYYYYY
posted by lalochezia at 1:19 PM on November 19, 2019 [5 favorites]


correctly identifying a mate of the appropriate gender

Teleology is a hell of a drug.
posted by Not A Thing at 2:01 PM on November 19, 2019


congrats sciatrix.
posted by ovvl at 8:09 PM on November 19, 2019 [1 favorite]


Thank you for explaining this! this is.. this just makes so much more sense?? that sexual dimorphism came after the development of sexual reproduction, as an adaptive evolutionary advantage. Right, that's what we're saying?

Very close! We're talking less about dimorphism itself and more about discrimination: that is, whether organisms bother to devote the resources to maintaining the ability "male" vs "female" apart when reproducing as well as maintaining the preference to avoid sex with anyone you aren't reproductively compatible with. So it's less about whether the two* sexes are physically distinguishable by sight or scent or sound and more about whether individual animals are a) paying attention to any differences, and b) acting on preferences with respect to that information.

That's one part of the argument. The next part is that we're also pointing out that engaging in SSB might not actually be a net detriment to your ability to reproduce at all, and that there's no reason the strength of preference only for reproductively compatible sexual partners might not vary over time, depending on context. After all, for many species, the rate limiting resource on successful reproduction isn't necessarily gametogenesis, particularly not for males.

*note that you may have multiple physical categories of animals within a sex. For example, it's common in fish to have both "territorial" male fish, who are large, aggressive, and often brightly colored, and also "sneaker" male fish who resemble female fish or are otherwise physically small and not very much like territorial males. Both produce sperm, but they aren't necessarily interchangeable categories for the fish.
posted by sciatrix at 7:38 AM on November 20, 2019 [7 favorites]


That makes me wonder then at what point a behavior becomes a "sexual" behavior. Or maybe that trying to draw strict lines for that is a mistake?

This was a hugely important thing in my mind when I was writing! And in fact, I spent a lot of very enjoyable* time playing the "define sexual behaviors" game when we were beginning to write, where I'd challenge people to define sexual behaviors and then bring up counterexamples that made the definition difficult. The definition we eventually settled on was, effectively, "if you would define this as a sexual behavior between two reproductively compatible individuals, it's a sexual behavior between two individuals who are not capable of reproducing, too." That's what we're getting at in Box 2.

Now, this is a hugely important point, because historically the same behaviors we define as sexual in different-sex pairs have often not been defined as sexual behaviors if they occur between same-sex individuals. This includes things like pair-bonding to raise offspring in birds, licking erect genitals in primates, anal penetration in giraffes, mounting and genital licking during estrus in cattle, and a wide variety of other behaviors. It seems beyond the pale that these behaviors would be defined as non-sexual if the animals involved in them were of different sexes, but there it is. Moreover--and this is another point we make--we often do define these behaviors as sexual if they include animals who are different-sex but not actually capable of reproducing, as in hybridization due to post-zygotic reproductive barriers. So defining sexual behaviors in the context of SSB can be particularly fraught because sexual behaviors are so often defined in terms of reproduction and fertilization, even though sexual behaviors involve wide ranges of behaviors invoking aggression, affiliative behaviors, motor behaviors, courtship behaviors, pair-bonding, and so forth.

*for me, not necessarily anyone else
posted by sciatrix at 8:01 AM on November 20, 2019 [10 favorites]


Yeah, I remember reading or being told that when two male dogs hump each other it's just one of them "displaying dominance" and even as a kid I was like "...but REALLY though? Like you're SURE about that?"
posted by showbiz_liz at 8:26 AM on November 20, 2019 [2 favorites]


I keep loving this more and more, sciatrix.
posted by schadenfrau at 8:53 AM on November 20, 2019 [2 favorites]


Also, wait:
*note that you may have multiple physical categories of animals within a sex. For example, it's common in fish to have both "territorial" male fish, who are large, aggressive, and often brightly colored, and also "sneaker" male fish who resemble female fish or are otherwise physically small and not very much like territorial males. Both produce sperm, but they aren't necessarily interchangeable categories for the fish.
I am reading this as “even fucking fish have figured out that gender is not sex”

And I’m hoping that’s right because it will make a great retort
posted by schadenfrau at 8:57 AM on November 20, 2019 [7 favorites]


You know what that puts me in mind of schadenfrau, is the old idea that each species of animal has a perfect or prototypical form against which individuals of the species should be compared. Evolutionary theory blew that up. And now it seems we're in the process of doing the same thing to the notion of a default model of sexuality where all non-hetero behaviors are abberations of the hetero template.
posted by showbiz_liz at 9:11 AM on November 20, 2019 [3 favorites]


We wrote an op-ed for Scientific American on the paper which might be a touch easier to digest.
posted by sciatrix at 1:58 PM on November 25, 2019 [10 favorites]




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