Sensitivity, charm and cleverness: very sexy

Ah, the life of the female giant Australian cuttlefish…males fight for her affections, and during the mating season she will have sex with 2-8 different males each day, with an average total of 17 copulations per day. She can be picky, too, and rejects most of the mating attempts (yet still manages to mate up to 40 times a day). It must be a good life.

Males have a rougher time of it, I would think. There are many more males than females, and so it’s a struggle to get access to one; the bigger, stronger males will guard females, acting as a consort, and use aggressive displays to chase off competitors. What to do if you’re a smaller, but clever male?

I know the answer to this one, recalling that when I attended DePauw University many years ago, they required all freshman women to live in a women’s dorm with rather restrictive visiting hours: the way around that was to dress up as a girl, which was much easier for the slender, smooth-featured young fellows than the burlier and hirsute football players. Cuttlefish are masters of mimicry, and they do something very similar.

a, An unpaired male (m) assumes female coloration and posture and approaches the paired female (f) while the consort (c) displays to an approaching large male (top right); note the conspicuous, large white arms, a sexually dimorphic male character. b, The female accepts a mating attempt by the female mimic as the consort continues to display to the other large male. c, The consort male allows the mimic to finish mating without interruption, even when he is not distracted; the other small ‘sneaker’ male has swiftly transformed into a female mimic as well.

There’s a recent short article with a very pretty movie of this behavior online, but it’s from an article in Nature from last year, and here are a couple of frames to illustrate what goes on. At the top is c, a big male consort, guarding the female. He’s got two competitors. At the top right is another big male, boldly swimming up to challenge him; he responds by flashing his tentacles at him. At the lower left, though, is another male, this one adopting the muted colors and demure posture of a female, sashaying up as if that gorgeous hunk of consort is irresistable.

In the middle panel, the consort is telling off the big interloper, while the the sneaky male is snuggling up to the female, and asking, “hey, do you want to…?” She says, “Yes!”

In the bottom panel, the two are going at it hot and heavy, while the consort looks on. It really needs a “WTF?” thought balloon over his head.

One of the strange things about all this is that the females really seem to like the sneaky males—they had a near-perfect record of sexual success, much better than the Blutos who try to strong-arm females into being sexual partners. There’s a lesson to be learned there, I think.

(via Thinking Meat News Blog)

Hanlon RT, Naud M-J, Shaw PW, Havenhand JN (2005) Transient sexual mimicry leads to fertilization. Nature 433:212.


  1. Andy Groves says

    Far from me to interrupt your cephalopod sexual reveries, but anyway……. here’s an example of sneaky male sexual behavior in midshipman fish, which actually have two male morphs, one big and butch, and the other girly and sneaky:

    Bass AH, Grober MS. Related Articles, Links
    Social and neural modulation of sexual plasticity in teleost fish.
    Brain Behav Evol. 2001 May;57(5):293-300. Review.

    The male fish sing as well. Isn’t that lovely?

  2. Mnemosyne says

    IIRC, doesn’t something vaguely like this happen with primates? As in, while the big alpha males spend their time fighting each other, the smaller males are busy sidling up to the females and inviting them into the bushes.

  3. Torbjorn Larsson says

    “There’s a lesson to be learned there, I think.”

    Let’s see; dress up as a female, sneak into a bar, get between a girl and the guys, and ask her for some LTC time? Yes, that will be a nice lesson, I think!

    I need some expert help to find a matching lipstick, though…

  4. jimBOB says

    Sometimes women like the “sensitive” male types. It’s like the old story of the gay guy with lots of women friends wishing he wasn’t gay.

  5. Caledonian says

    Why do some males continue to utilize the bullying strategy, though? Is it just that, given their physical bulk, they couldn’t make the sneaky strategy work?

  6. Anton Mates says

    Why do some males continue to utilize the bullying strategy, though? Is it just that, given their physical bulk, they couldn’t make the sneaky strategy work?

    In fish, at least, the success of sneaking seems to be density-dependent–you need a fair number of big males around busy beating on each other so that you can sneak in during all the commotion. If almost every male’s sneaky, the one big male in the area has time to check them out, spot the deception and send them packing. So the morphs tend to reach an equilibrium.

    Dunno if that’s how it works for cuttlefish, though.

  7. Caledonian says

    Is sneakiness still preferred by the females in populations where the largest, least-female-like males have been removed, I wonder?

  8. Carlie says

    Oh, my word! I just covered alternative male sneaky mating strategies in my evolution class last week. I guess I’ll have to do a quickie update for them tomorrow…

  9. Loris says

    With primates it depends on the taxa. For instance, chimps have safaris where females sneak off willingly with a subordinate male. Ring-tailed lemur females are dominant within the social hierarchy. When they come into estrus they will entice males to have scent fights for access. While two males are already fighting over her, the female will mate with another male.

    Orangs are really different. There are two kinds of males. The big males who look like traditional orangs with the big cheek pads and such have a territory that overlaps several females. He will defend those females against intruding males. The other kind of male is small and retains the appearance of a juvenile (in fact they were thought to be juveniles until recently). These males will sneak into the territory of a female already under the protection of a big male. The small male forcibly copulates with the female (she’s screaming bloody murder to attract her preferred mate to save her). If the big male hears the female, he will come and force the intruding small male off of her. One of the really wierd aspects of this behavior is that the small males are usually trying to copulate with females that are not in estrus and are not receptive. They’re not sneaky in the same way as the cuttlefish males.

  10. CCP says

    More and more of these amazing alternative-strategy stories are coming out all the time (Roughgarden refers to them as different animal “genders;” I dunno). My favorite is Barry Sinervo’s lab’s stuff with side-blotched lizards. They have identified three different male morphs that differ in both chin color and behavior: Orange-throated males are superdominant and polygynous, defending large territories that contain the homeranges of several females; blue-throated males defend smaller, 1-or-2-female-size territories, and yellow-chinned males are female-mimicking sneaky fuckers, like the cuttlefish. What’s so cool is that, mating-success-wise, orange beats blue (aggressively repelling them from the orange superterritories), but yellow beats orange (sneaking in while the territory owner is off somewhere else defending a border), and blue beats yellow. It’s a natural rock-paper-scissors game, with the success of each male morph depending on the current density of the other two morphs, and as a results there are regular, cyclic changes in the frequencies of the three morphs. (There are also underlying physiological correlates). So cool.

  11. Richard Eis says

    Is there an age issue here? the younger they are the more easily they appear smaller and more feminine. That would also explain their success with the females.