Amazons

Nature-Nurture-Noise (4)

In the 1980s, if you mentioned, even casually in passing, that the fish you observed had distinct personalities, you would have been accused of gross anthropomorphism, that is, an unwarranted projection of human mental states onto animals. I say this from experience. The fish species whose personalities I had noted is the Midas cichlid (Amphilophus citronellum), so called because of the yellow-gold coloration of some adult individuals. The Midas cichlid is a very large cichlid—males weigh over two pounds—native to the Great Lakes of Nicaragua, where renowned ethologist and ichthyologist, George Barlow (University of California, Berkeley), had first collected them in the early 1960s. Ever since, a colony had been maintained in the courtyard at the basement level of the Life Sciences Building. They were the main focus of George’s behavioral research.

Those individuals that were to be used in experiments, or to breed, were transported to a fish room—containing around thirty 100-gallon tanks in George’s third floor lab. It was there that I first noticed the marked individuality of these creatures. One striking example was a large golden male who had learned how create waves that would eject considerable amounts of water through an opening on top of the tank at the front end. He did so by moving rapidly toward the front, then turning suddenly sideways when he was about a foot away. Since he was housed on the third level (about eye level), he could create quite a splash on the floor. But splashing was not his goal; he waited until he could see that someone was kneeling below so that his waves could crash on a human. Even when it came to his human targets, he was discriminating, having a particular animus for the maintenance guy who cleaned his tank. After enduring that indignity, he would wait until his nemesis got to a tank immediately below before he made his move.  He was the only fish in the room that engaged in this behavior. What is that if not personality.

I observed less dramatic but more consequential evidence of individual personalities when pairing males and females for breeding. Compatibility was everything and it could not be predicted, except from previous breeding records. (Each individual had a numbered tag.) If you placed a random male and female together, chances were they would fight rather than mate. One of my favorite female breeders was particularly picky. In fact, she would only breed with one particular male. This male wasn’t obviously physically superior to other candidates; his only distinguishing characteristic was a rather laid-back manner for such an aggressive species.

Though my own research concerned social control of sexual development, I decided to do an experiment on behavioral individuality on the side. I took some newly weaned (this species does actually wean) fry from the picky female and her preferred mate as my subjects. The subjects were tested monthly for aggression and fear in various contexts. They showed remarkably consistent individual differences in some of these tests over the course of two years, during which they sexually matured. When it came time to publish the results in 1989, I was confronted with the problem of a title. I was tempted to use the term “personality” in the title but was discouraged from doing so. So, I used the more technical-sounding term, temperament, instead.

Today, I wouldn’t hesitate to use personality in the title. In the behavioral sciences now, personality is quite in vogue, for fishes as much as mammals. Much of this research focuses on the evolutionary significance of personality variation and hence the genetic component of personality; but there is a lot more at play in personalities than genes.

Molly Personalities

A favorite species for neophyte tropical fish keepers is called the black molly, a melanistic form of the common molly (Poecilia sphenops). I acquired some, with saved allowance, when I was quite young. The common molly, along with guppies, platys and swordtails, belongs to a family of fish called Poeceliidae (pee suh LEE uh dee), noteworthy for, among other things, internal fertilization and the bearing of live young, both atypical for fishes. Though I soon expanded my repertoire of freshwater tropical fish, I retained a keen interest in mollies and their kin. When an undergraduate I learned of an especially intriguing member of the family called the Amazon molly. Amazon mollies are not named after the river, rather, the moniker refers to the mythical female Greek warriors, every bit the equals of Greek men when it came to strength and martial skills. No men were allowed in Amazon society; they only reared their daughters; any sons were returned to their biological fathers who lived elsewhere and whose company the amazons sought solely for procreational purposes—presumably with a minimum of foreplay—after which they were immediately dismissed. The Amazons strenuously avoided male contact, except in battle.

The Amazon molly is aptly named in this regard. They too minimize the role of males in their lives, but to an even greater degree heir human counterparts. The Amazon molly is an all-female species that birth only female offspring through a process called gynogenesis. Amazon eggs develop into full blown Amazons without the spermatic genome. Unfortunately, from an emancipatory perspective, they still require fertilization of a sort, to initiate development, to kick things off as it were. Though required to stimulate the development of the unfertilized egg, the genes in the sperm are excluded from the zygote, which is how Amazon mollies manage to remain a clonal species.

But if Amazons are an exclusively female species, from whence does the sperm derive? Turns out it derives from any one of a number of other molly species that have retained their sexuality, ergo males. But why would a male molly of another species deign to inseminate an Amazon, only to have its genes excluded? It goes against the evolutionary ethos. If you have watched male mollies as I have, the answer becomes clear. Males from all species in the family to which the molly belongs are unquenchably horny. They flash their penis analogs, called gonopodia, constantly in their unremitting pursuit of females, which to the human observer and probably the female molly constitutes extreme harassment. Female mollies must expend considerable energy to avoid unsolicited male molly genitals.

So, it is not surprising that wherever two species of molly co-occur, there are lots of hybrids. Indeed, the parthenogenic amazon molly derives from one such hybrid individual. Male mollies just can’t help themselves; any properly situated generic molly orifice will do. Amazon mollies take advantage of this male propensity. In essence they reproductively parasitize the males of other molly species.

Personality Variation in Amazons

It may come as a surprise that behavioral propensities of fishes can be measured along much the same dimensions as those of mammals, from mice to humans. Some of the more important behavioral dimensions include sociability, aggressiveness, boldness, and reactivity (fear response) to novel stimuli. Mollies vary along all of these dimensions.

Most personality research in non-human animals assumes a large genetic component for personality traits and syndromes. Genes, though, cannot be the source of variation in Amazon mollies, barring mutations. But Amazons have been around for around 200,000 years, according to the latest estimates, time enough, according to some, for a significant number of mutations to accumulate. So genetic differences cannot be completely discounted as a source of individual personality differences.

But within a single brood of Amazons genetic identity can be assumed. Moreover, all member of the brood experience the same environment within the Mother mollies womb analog until they are unceremoniously ejected to meet their fate without any maternal assistance. It was with these facts in mind that the following experiment was conducted by David Bierbach, Kate Laskowski and Max Wolf at the Leibniz Institute in Berlin, Germany.

Amazon fry were removed from the natal tank immediately after their birth. They were then reared in one of three ways: some in small groups from the outset; some in isolation for seven days, then in small groups; some in complete isolation for the duration of the experiment. All fish were then assessed, individually, at 49 days (seven weeks) for their exploratory behavior in a novel environment. This behavioral assay is like the one used by Kempermann and his associates in their study of isogenic mice discussed in a previous post (The Third Factor).

The clonal mollies reared in social isolation showed remarkable variation in their propensity to explore. What about those reared with their clonal sibs. Like many animals, mollies form social hierarchies. It is natural to expect that the Alpha mollies would be bolder, and hence more exploratory in the novel environment than the omegas. If so, the socially reared clones should evidence even more variability--the exploratory scale-- than those reared in isolation throughout. Such was not the case. Those mollies reared in isolation throughout were just as variable as those reared under more normal conditions socially.

To summarize, much as in Gartner’s mice, environmental enrichment—in this case, social-- didn’t increase behavioral variation. Hence, the variation in exploratory behavior was independent of both genetic background (they are effectively clones) and the environment. Put another way, the behavioral individuality of these amazons has other sources than genes and environment as generally conceived. The source of this variability must be chancy fluctuations in some developmental processes prior to their birth. Given that the variation is behavioral (personality), the brain would be an obvious to look for the developmental randomness. The brain, as I will discuss in a later post, is the organ most susceptible to random perturbations.