HOMOSEXUALITY AND HEMAPHRODITISM IN TERRESTRIAL INVERTEBRATES

INTRODUCTION

   As you probably are aware, Facebook was awash with red and pink equality symbols to promote marriage equality. It coincided with the United States supreme court hearing two marriage equality cases - Proposition 8 from California (which bans same-sex marriage) and DOMA (the Defense of Marriage Act). Seeing as this is the first official post from The Skeptical Entomologist, it seems fitting to honor marriage equality by dispelling one very common myth, at least in America and in conservative/fundamentalist religious culture: that homosexuality is a choice, and that it is not natural. Of course, being an biologist specializing in entomology and arachnology, I am going to use terrestrial invertebrates to argue that such a position is not only empirically false, but that it can be found in nature, and can be demonstrated in the laboratory. 

   Of course, many insects and arachnids do not reproduce in the way that humans do (that is, through direct sexual contact). Scorpions, for example, along with several other species (most notably spring tails), engage in indirect sexual contact. Male spiders, on the other hand, do engage in direct contact to fertilize the female, although he uses his pedipalps, rather than a penis, to get the job done. In some insects, such as bed bugs, the male not only uses a penis, but drills through the female's exoskeleton to fertilize her. And then there are animals such as worms and slugs, who are hemaphroditic; while worms may line up male-female genitalia, the infamous tiger slug (Limax maximus) passes sperm to it's mate through penis-penis contact.

GENES AND HOMOSEXUALITY IN  Drosophila melanogaster

   Of all the animals we know the most about, perhaps the one most well known to scientists is Drosophila melanogaster, also known as the common fruit fly or vinegar fly. The complete genome for D. melanogaster was first published in 2000, and is used as a model for developmental genetics in higher eukaryotes (Adams et al., 2000). Therefore, if any question to the "naturality" of homosexuality were to be scientifically addressed, it would make sense that the vinegar fly would be used as a model organism. 

   Now, I know what any naysayer (don't call yourself a skeptic, because, honestly, you aren't) may be thinking right now - that fruit flies are so far from humans that any research done on them could not possibly be attributed to higher level organisms, including humans. We should probably begin our examination of fruit fly homosexuality by addressing such a concern. D. melanogaster as a model organism for humans has been well established, and, when compared, 714 disease genes (approximately 77%) from humans matched with 548 disease genes from vinegar flies (Reiter et al., 2001).

   Now that we have established that vinegar flies are widely acknowledged as a model organism for higher animals, we should probably address why they are such good animals for laboratory research: their rate of reproduction. Each individual fly has a life span of, on average, thirty days, allowing up to twelve generations in one year. Developmental time for the embryos, under ideal conditions, is 8.5 days, and a female can lay up to four hundred eggs. This all creates, in short, an organism which is rather handy to have around the laboratory. 

   D. melanogaster is valuable to the dialogue of homosexuality in animals (humans included) because  they have been used to experimentally determine whether homosexuality is caused by intent (such as choosing same-sex partners over opposite-sex ones) or whether such an inclination is arbitrary (no such choice was made by any individual). But first let's look at the rates of vinegar fly homosexuality in natural populations. 

   In the wild, roughly eight percent of all observed D. melanogaster flies have been found to exhibit at least some form of homosexual behavior, and it has been noted that immature flies appear to be attractive to mature males (Napolitano, Tompkins, 1989). In the laboratory, it has been discovered that homosexuality in D. melanogaster was caused by a gene located at 91B, which was also found to be the location in the fruit fly's genome responsible for the bisexuality phenotype (Yamamoto, et al., 1996). By manipulating this area of the genotype, scientists have been able to raise the rate of male homosexuality from 8%, as seen in wild populations, to as much as 90%. This, indeed, would support the case that homosexuality is not a choice, but rather the result of genetics. It is as natural in fruit flies as the color of their eyes, and it would, therefore, be as natural in humans as is our height or skin tone.

TWO WELL KNOWN HOMOSEXUAL INSECTS

Dragonflies: Hagenius brevistylus, Gamphus lineatifrons, & Gamphus viridifrons

   D. melanogaster is not the only insect in which members have been observed copulating with the same sex. The iconic dragonfly is known for it's aerial courtship displays, and it, too, has been observed in homosexual acts. The unique thing about dragonflies is that they do not have to be caught in the act to determine if they have partaken in homosexual relations. As is well known, during mating, the male dragonfly grabs the female's occipital area with the "clamp" found at the end of his abdomen; this often leaves telling scars. This tell tale sign has also been found, not surprisingly, on male dragonflies. In the species Hagenius brevistylus, for example, 129 individuals were sampled (101 males, 28 females); of these individuals, 89% of females and 83% of males were found to have "clamp" scars in the occipital area (Dunkle,1991). In another species (Gamphus lineatifrons), 49% of the 71 sampled males were found to have scars, while in another species of the same genus (G. viridifrons), 15% of the 48 sampled were found to carry scars (Dunkle, 1991).

Bedbugs: Cimex lectularius

   A species of bed bug, Cimex lectularius, has also been found to take part in homosexual copulation. This seems to be due to the attraction of a male C. lectularius to a recently fed individual, which, naturally, would result in at least some basal homosexual coupling. The male penis is needle-like, which the females have counterevolved a special organ, known as a spermalege, to cope with the male's needle-like member. Because males do not have such an organ, they produce alarm pheromones when homosexual copulation commences, as C. lectularius copulation is often violent and causes harm; this helps to reduce homosexual encounters in the population (Ryne, 2009).

"Functional" homosexuality in the parasitic wasps

   Another species of insect found to engage in homosexual behavior is the parasitic wasp Psyttalia concolor. It has been hypothesized that young males who are courted by mature males may have have more reproductive success as an adult (Benelli, Canale, 2012), although no difference has been discerend between individuals which were courted by males as opposed to those courted by females while immature (Benelli, Canale, 2012). It has also been observed that, among some species of parasitic wasps, males occasionally attempted to mate with males who were already mating with a female. In these species, females use pheromones to attract males, and when a male mates with a female, the pheromone is passed to him. To the male wasp initiating the homosexual contact, he is under the impression that he is mating with a female wasp. 

   However, it has been observed that when the original male has finished copulating with the female, he will become submissive to the male which initiated same-sex copulation. It has been hypothesized that this allows the female to "escape", as it were, with only the sperm of the original male wasp. In this way, by allowing another male to mount him, the original male ensures that his genes - and only his genes - are passed onto the next generation. 

 THE TIGER SLUG - HOMOSEXUAL RELATIONS BETWEEN HEMAPHTODITIC INDIVIDUALS

   Perhaps the most beautiful of any sexual practice in the invertebrate kingdom is the mating ritual of the tiger slug, Limax maximus. It is also unique because the slugs are hemaphroditic, and unlike other hemaphroditic organisms such as earth worms (which line up female-male genetalia), the sperm is passed to the other slug from penis to penis. Not only is it the most visually stunning mating ritual in the animal kingdom, it also happens to be one of the most prevalent homosexual practices. 

   As one may imagine, it an organism is hemaphroditic, it may be somewhat difficult to label them with any sexuality. An earthworm, for example, may be said to heterosexual as the copulation occurs with male-female parts, and yet it could be argued that they are homosexual, as both individuals have both sets of genitalia. Limax maximus, however, uses only the penis during mating, which then uses the sperm from the other individual to fertilize itself. It may be said that the tiger slug reproduces essentially through homosexual copulation. 

WHERE DO WE GO FROM HERE?

   Now that we've established that homosexuality exists in insects and other invertebrates, we can rightly ask of ourselves: where do we go from here? Now that we know, how do we apply it? It's quite simply, really. Now that we know that homosexuality is not a chosen lifestyle (thanks to the vinegar fly) and that it occurs naturally in all animals, from dragonflies to humans, perhaps we can move on to more pressing matters. Science is a wonderful tool to be used to better the lives of ourselves and to improve the world in which we live, to better understand our place in the universe. Our knowledge allows us to look not only at humans who are different from us, but also at other animals, including insects, and realize that, despite differences which may be incredibly large and seemingly insurmountable, we are not so different after all, and there is always a way to appreciate each other and live in peace.