Sunday, February 1, 2009

Sex with Flexible Partners #3

Wrapping-up hermaphroditism as a general topic, in this edition of Sex with Flexible Partners the relative reproductive values of male and female gametes will be reexamined in the light of dynamic social settings. For those new to this series of blogs, occasional flashbacks to broad ideas and concepts may necessitate the reading of the inaugural article found here, as well the precursor to this current writing found here. If, by chance, the title “sex with flexible partners” is the primary reason for arriving at this site – rest assured – explicit lifelike images are included below!

Moving towards the subject at hand, through several previous examples, such as with representative Chalk Bass (Serranus tortugarum), Hamlet fish (Hypoplectius), polychaete worms (Ophryotrocha puerilis) and freshwater snails (Helisoma trivolvis), the presence of heterogamy resulted in either the changing of sexes or the development of complex behaviors in hermaphroditic organisms. These dynamic strategies were adapted as a means of more efficiently managing the costly production of female gametes. The idea of relative gamete values between male and female reproductive cells pointed to the conclusion that as a rule, “eggs are expensive, sperm are cheap.” Although this rule holds true under the majority of circumstances, there are conditions wherein the comparative value of sperm increases relative to that of ova and thereby pushes functional gender roles of some hermaphrodites in novel directions.

Many sequential hermaphrodites, such as clownfish (Amphiprion), exist in complex social environments in which multiple organisms establish communal groups and engage in cooperative behaviors. Through interaction with multiple individuals, circumstances can arise that directly effect the reproductive success of not only a single mating pair, but also the fecundity of all members of the group. Often a group stake in local fecundity results in a change in the values normally associated with male and female sex cells. As exemplar of group interest in reproductive success, the common clownfish (Amphiprion ocellaris) exhibits just such a dynamic.

[Amphiprion ocellaris]

Amphiprion ocellaris, probably best known as “Nemo” from the 2003 feature animated film “Finding Nemo,” is a protandrous sequential hermaphroditic fish that combine as groups in which a single dominant male pair-bonds with a single female and then cohabits with several smaller, sexually immature males. For the sake of clarity, it is important to bear in mind here that the reproductive biology of the species Amphiprion ocellaris is being discussed, not the cartoon character Nemo’s social preferences – libel is to be avoided.

The smaller male members of the group don’t attempt to mate with the female, they’re reproductively immature, rather they stick around because of the protection offered by the dominant male who remains at guard and patrols the host anemone in which they all reside. If the female clownfish should die or be killed, rather than risk the loss of the dominant male’s protection – he would need to leave the anemone in pursuit of a new mate – the largest of the immature male anemone-mates will undergo a sex change and take up the role of reproductive female thereby insuring the dominant male's continued presence. If, instead of loosing the group’s reproductive female, the dominant male is killed or dies, then the female vacates her egg laying responsibilities and undergoes a sex change to replace the male. Her position as reproductive female will later be taken-up by one of the immature males as described previously.

In the clownfish example, social pressures linked to the protection of the group complicated the process in which hermaphroditic fish chose a functional sex role - even to the extent of abandoning the all important task of egg production - these complications also occur under circumstances in which the creation of sperm becomes more critical than does manufacture of ova. Communal groups of blue headed wrasse (Thalassoma bifasciatum) sometimes encounter just such a state of affairs.

[Thalassoma bifasciatum]

“Blueheads,” as Thalassoma bifasciatum can commonly be referred, are protogynus sequential hermaphrodites that form large, male dominated harems in which a group of females establish a female-only hierarchy. The male controls the group, provides protection and manufactures sperm; the largest female in the group is the primary egg producer and to a certain extent controls the lesser females. Because blueheads live in groups with highly biased sex ratios – many females, one male – eggs are “a dime a dozen” – they’re cheap. If the lead reproductive female should die or be killed, the next largest female in the hierarchy will hurriedly succeed her and take over as primary ova supplier with little fuss. Whereas there are an abundance of females and only a single male, the sperm he contributes is of greater importance to the group than are eggs. The eggs are expensive, sperm are cheap rule - although still valid in regards to resource allotment for an individual - in this social scenario no longer holds true. If the dominant male bluehead should be killed or die, it’s well worth the expense of undergoing a sex change to replace him, and this is precisely what the lead female does, she changes to a male and takes over the harem.

Taking over a harem is by no means an easy job, there is plenty of risk involved in defending the group against predators and out maneuvering the continuous onslaught of rivals vying for the throne; but taking the male role benefits both the individual and the group as a whole because it streamlines the passing of genetic material to the next generation. Another species of reef fish, Trimma okinawae, will even forego the hassle of finding a new harem, should his be lost to a rival; he’ll just join another one – as a female.

[Trimma okinawae]

Social dynamics can have traumatic impact on the physiological and behavioral characteristics of organisms, but it’s important to keep in mind that no single phenomenon is responsible for all biological adaptation. Evolution works along a vast continuum of gradation; the physical environment, resource availability and social constraints are but a few of the uncountable factors carefully weighed by Natural Selection.

There are exceptions to all of the examples listed in this discussion, and there are those organisms that sneak, manipulate and cheat the system to their advantage, some of these cases will be the focus of future installments, but for now it’s a safe assumption that the incredible sexual flexibility exhibited by hermaphroditic organisms has proven to be an effective strategy in assuring reproductive victory over rivals.

P MUNDAY, P BUSTON, R WARNER (2006). Diversity and flexibility of sex-change strategies in animals Trends in Ecology & Evolution, 21 (2), 89-95 DOI: 10.1016/j.tree.2005.10.020

Shohei Suzuki, Kyoko Toguchi, Yoshimi Makino, Tetsuo Kuwamura, Yasuhiro Nakashima, Kenji Karino (2008). Group spawning results from the streaking of small males into a sneaking pair: male alternative reproductive tactics in the threespot wrasse Halichoeres trimaculatus Journal of Ethology, 26 (3), 397-404 DOI: 10.1007/s10164-008-0102-3

Verena S. Brauer, Lukas Schärer, Nico K. Michiels (2007). PHENOTYPICALLY FLEXIBLE SEX ALLOCATION IN A SIMULTANEOUS HERMAPHRODITE Evolution, 61 (1), 216-222 DOI: 10.1111/j.1558-5646.2007.00018.x


  1. The intricacies of it are mystifying. It's almost like the quantum physics of biology: it almost defies logic in one sense, but is also perfectly logical on the other.

  2. I'm confused about the clownfish. How can the young be called "male" if they're sexually immature, and sex is not fixed? Wouldn't that make them neuter?

  3. Sorry that this has to be so short, but I’m in the process of packing to go to the field… I’ll be back Friday morning and can provide a better explanation then, but;

    Amphiprion ocellaris is a sequential hermaphrodite as opposed to a simultaneous hermaphrodite, it only takes on the function of one sex at any given period; If my memory serves me correctly it takes 7-14 days to change between sexes. If you get time take a look at “Sex with Flexible Friends #2” – it compares sequential to simultaneous and talks about functional roles.

    With the common clownfish, Amphiprion ocellaris, all fish are born male with the color patterns and body size associated with being the male sex, only later do they become female.

    Thanks for the posts – I can clarify more on Friday.

  4. it only takes on the function of one sex at any given period;

    I understand that, but from what I understood from this article, it sounds like, in any given group, there's only a single member taking on the functions of male, and a single member taking on the functions of female, while the others aren't taking on either function. If they're not producing sperm or ova, why would they be called male?

    With the common clownfish, Amphiprion ocellaris, all fish are born male with the color patterns and body size associated with being the male sex, only later do they become female.

    Okay, I think I understand it now. So, although they're not functionally either sex, they resemble the functional males rather than the functional females, and this is why they're assigned to the male sex? Or am I completely misunderstanding this?

  5. ranka,

    I think you’ve got it, but keep in mind that the intent of defining an organism as “functional” in regards to a sex role is to better delineate the behavior of a reproductively mature organism, not to describe sexually immature members of a group.

    In the case of Amphiprion ocellaris, it’s not so much that the subordinate males are gender neutral (they are male), rather it’s that they’re sexually immature and do not take on any reproductive role – because they don’t reproduce, they can be thought of as without “sexual function.” Later, when the subordinate males begin to reproduce, hormones will drive them towards one gender or the other, when this occurs they will take on a functioning sex role.

    Thanks again.