Sex with Flexible Partners: Socio-Ecological Reproductive Strategy #1

Reproductive strategies and natural mating systems have long been a favorite topic of those with interests in the areas of ethology, ecology and evolution. From the call of the nightingale, which is at the same time both alluring and manipulative, to the merging of circulatory systems by the male and female anglerfish, the myriad of processes employed by organisms in bringing forth future generations are as fascinating as they are bizarre. It is because of this fascination that this short essay is written. It represents the first of several that will provide a précis of the range and disparity in sexual strategies utilized by the natural world in meeting the demands of one of its prime drivers – sex.

In contrast to more formal literary approaches, this initial essay will move historical context to the backburner as a reserve for future conversation and jump-in headfirst by discussing one of the more unique tactics applied in promoting fecundity; a reproductive tactic that’s applied by a vast array of organisms from plants to annelids to vertebrates - hermaphroditism. More specifically, this first installment will discuss a type of hermaphroditism called “simultaneous hermaphroditism.”

Hermaphroditism, when used in the context of natural history and behavioral ecology, doesn’t hold precisely the same meaning as it does when used in popular – non scientific – conversation. In terms of reproductive strategy the term can be used to describe one of two situations.

In the first scenario, called “simultaneous hermaphroditism,” organisms exhibit both male and female genitalia – they are 50% male and 50% female – and are able to produce the gametes of both sexes, both female ova and male sperm. In this instance, although able to produce both sperm and ova, self-fertilization is avoided through production of digestive enzymes that act as a barrier, destroying one of the two gametes. This type of hermaphroditism is practiced by several species, including a variety of nudibranchs (Nudibranchia) and the Chalk Bass (Serranus tortugarum).

[Nudibranchia -top; Serranus - bottom]

Energetically speaking, simultaneous hermaphroditism as a strategy is most useful for organisms that exist in populations of very low density, where the cost of searching out a mate is greater than the expense associated with maintaining two independent reproductive systems. Ecological benefit occurs because when seeking a mate, either a male or female will serve the reproductive function, thus the chances of finding a partner are twice as good as they would be if forced to locate a member of a specific sex.

However, being two sexes simultaneously does have its difficulties, especially when negotiating with potential mates in regard to total parental investment. Although the chances of locating a mate are improved if gender isn’t a concern, the total investment in reproductive effort can be a point of discord. Like other vertebrate sex cells, the “female” and “male” gametes (here female and male refer to the sex role undertaken at the time of mating) in fish are different sizes, this is called anisogamy or heterogamy.

Female gametes (ova) are larger in size than that of the male gametes (sperm). They’re larger because they must provide not only the “female” contribution of genetic material to the developing zygote, but in addition they must also supply the zygote with all of the nutrients and protection required during embryological development. Spermatozoa by contrast are merely vehicles for delivering the male genetic compliment and are less costly to manufacture and deliver; plainly stated, sperm are cheap, eggs are expensive.

Considering the resource investment involved in gamete production, when two simultaneous hermaphrodites meet for the purpose of reproduction, which member is going to take on the extra burden of producing eggs and which is going to provide the “cheap” sperm? What’s to prevent one fish from “cheating” the system by not providing eggs and only producing sperm; thereby reserving resources while spreading his genetic compliment at the expense of another’s egg investment?

Hamlet fish (Hypoplectius) resolve the egg stand-off through a process called “egg trading.” During egg trading both fish first subdivide their egg clutches into individual parcels for ease of dispersement. As breeding commences, one fish initiates mating by releasing a single egg parcel; seeing this, the opposite fish readily fertilizes these eggs with sperm. Next, the roles reverse. The fish that initially fertilized the eggs with sperm now renders one of its egg parcels to the fish which provided eggs during the first exchange; as in, “you scratch my back, I’ll scratch yours.”

[Hypoplectius]

If the Hamlet that provided sperm during this first exchange should refuse to supply one of its parcels in return, the courtship will be broke off prematurely and mating will cease with only a few eggs fertilized. If however, the initial sperm supplier “plays fair” and then produces a parcel for the initial egg maker to fertilize with its sperm, the process will continue, back-and-forth to the mutual benefit of both fish, ultimately resulting in greater numbers of total eggs fertilized. Because of this unique dynamic, egg trading is often used as an example of reciprocal altruism and as an analogy when discussing biological “game theory” – but these are topics for other times.

The second type of hermaphroditism is called, “sequential hermaphroditism.” Sequential hermaphroditism means that an organism literally becomes a member the opposite sex! An organism is born as one gender, with the sex characteristics and reproductive organs of a single sex, but then it undergoes a “sex change” in which the full range of hormones, morphology, coloration, behavior and social position that are normally associated with the opposite sex are phenotypically expressed. Males literally become females, females literally become males.

In some instances, sequential hermaphrodites undergo a change in sex at a predetermined age in conjunction with the normal growth and maturation process, but in other cases this transition occurs in response to an environmental or social factor. Furthermore, this switching of sexes isn’t limited to a one time occurrence; a single individual can change repeatedly – back and forth, again and again.

In order to keep the length of these ramblings to a readable minimum, sequential hermaphroditism will be the topic of the next installment.

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

Eric A. Fischer (1987). Mating behavior in the black hamlet — gamete trading or egg trading? Environmental Biology of Fishes, 18 (2), 143-148 DOI: 10.1007/BF00002602