Sexy Snails and Expensive Males

What are males good for? A study published this month in the journal Molecular Biology and Evolution provided new insights into one of the many benefits of sexual reproduction. The research, conducted out of the University of Iowa’s Roy J. Carver Center for Comparative Genomics, examined the mitochondrial genomes of a freshwater snail species in order to compare the rates at which genetic mutations accumulate during sexual and asexual reproduction.

The freshwater snail Potamopyrgus antipodarum is unique in that it can reproduce either sexually or asexually. In their native range male and female snails reproduce via sex; however, in places like the U.S. populations of P. antipodarum are clonal – they’ve been established by invasive and asexual females. By counting-up mutations and comparing the mitochondrial DNA of populations derived from sexually functional males to those populations founded completely by parthenogenic females, researchers were able to demonstrate that genetic recombination through sex effectively removed mutations from the snail genome.

The removal of potentially harmful mutations (‘purifying selection’) from a population is a benefit that may help explain why the expenses associated with sex are maintained by evolution. See, males do have value!!!

Neiman, M., Hehman, G., Miller, J., Logsdon, J., & Taylor, D. (2009). Accelerated Mutation Accumulation in Asexual Lineages of a Freshwater Snail Molecular Biology and Evolution DOI: 10.1093/molbev/msp300

Twisted Penises, Convoluted Vaginas and Really Ducked-up Sex

Wow, I really had a tough time coming-up with a title for this post! There were so many possibilities…

In the December 23rd edition of the journal of the Proceedings of the Royal Society B, several scientists from Yale University detailed their recent experiments into the coevolution of male and female duck genitalia. Specifically, the researchers wanted to evaluate whether or not the physical morphologies exhibited by duck penises and duck vaginas provided evidence of ducks being actively engaged in a sexually antagonistic ‘arms race.’ In hopes of resolving this reproductive riddle, the folks from Yale traveled to a commercial duck farm in California, while equipped with artificial duck vaginas, mineral oil and a high speed video camera.

Sexual conflict arises when the strategies used to optimize reproductive fitness differ between the males and females of a species. In the case of muscovy ducks, like those used in the Yale research, the strategy of the male is to mate as frequently as possible, and with as many different females as he can find – even if sexual coercion is the only means available to achieve these goals. Conversely, the strategy of the female is to select only the healthiest of males as reproductive partners and to outright reject all those deemed unworthy. Because the male and female strategies are in conflict – quantity vs. quality - both sexes have undergone adaptations to out-maneuver the opposite gender. In this back-and-forth battle for reproductive victory the process of sexual selection has discovered an affective tactic - to change the physical shape of the duck’s genitalia.

In addition to being one of the few birds with a penis at all, the phallus of the male muscovy duck is physiologically and morphologically very unique. Unlike the penises of most mammals, which when erect are hydraulically rigid and supported by axial-orthogonal layers of inextensible collagen fibers, the penis of the muscovy has an arrangement of supportive fibers that allow for complete flexibility while erect. Besides being highly limber, the shape of the muscovy’s twenty centimeter long penis is ‘twisted’ forming a distinctive counter-clockwise spiral. These functional traits allow the male to very quickly insert into the female during copulation.

The speed at which copulation occurs is of vital importance to the male, it gives him the ability to inseminate even those females that actively defy his advance. Physical resistance is minimized because the male can insert his penis at a speed of about 1.6 meters per second and complete insemination in just 0.36 seconds – that doesn’t leave much time for fighting. Since the male’s seemingly invincible swiftness eliminates combat as a pragmatic brood planning option, the female line has employed an anatomical counter adaptation to ensure its continued mate choice.

As a defensive escalation in the muscovy’s inter-sexual arms race, the female has undergone adaptation for a counter armament – she’s changed the shape of her vagina. The female duck’s vagina can be found to exist in one of two possible shapes, either with a 135-degree bend, or with a clockwise ‘twist.’ During forced copulations, the morphology of the vagina functionally prevents the male’s penis, or his sperm, from entering sufficiently far into the reproductive tract to result in fertilization. However, when the female muscovy is receptive to a male suitor – when SHE chooses a mate – she actively facilitates the sexual congress by taking on a body posture with an elevated tail. The elevated tail, in combination with muscular contractions, permits the male duck to penetrate further into the reproductive tract and thus improves the likelihood of successful fertilization.

To uncover the fascinating story of co-evolving duck genitalia, the researchers from Yale presented aroused males with replicated duck vaginas. In conducting the experiment, female ducks were placed in a cage with a male, once the male initiated a mounting behavior, the female was quickly removed and the male was filmed with a high speed video camera as he inserted his penis into one of four different shaped molded test-tubes. The mineral oil covered test-tubes either had a straight shape, mimicked the male’s penis with a counterclockwise twist, or they had a female-like clockwise twist or 135-degree bend. After analyzing the film, the scientists discovered that the replicated vaginas that matched the shape and dimensions of real-life female muscovies effectively blocked the male’s penis from reaching very far into the test-tube.


Patricia L. R. Brennan, Christopher J. Clark and Richard O. Prum (2009). Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genitalia Proc. R. Soc. B

The Circumvention of Compulsory Sex

Males are sexually coercive. During initial encounters with the opposite sex, they will go to great lengths to impress and entice; they’ll offer gifts, sing, dance, and do whatever else is necessary to win a female’s affections. However, should these preliminary advances be rejected, the males from a multitude of different animal species will unhesitantly apply the tactics of deceit, intimidation and even brute force to satisfy their reproductive drives.

Through forced couplings males enhance the spread and flow of their genes within the larger gene pool. By mating with both those females that accept his flirtations and those that don’t, the total number of a male’s sired offspring in the population is increased. This strategy provides the male with a reproductive leg-up over his rivals - the other males in the population. Energetically speaking, the tactic of repeated mating comes at a bargain price, because unlike females, males don’t usually incur the taxing reproductive expenses associated with pregnancy, tending to offspring, or for that matter even production of female reproductive cells – the ova.

In most vertebrates, female and male gametes differ in size and structure; this phenomenon is referred to as anisogamy. The female gametes (ova) are larger in size than that of the male gametes (sperm). Ova are larger because, in addition to containing the female’s DNA, they provide all of the nutrition and protection required for the resulting embryo’s development. Spermatozoa by contrast are merely vehicles for delivering the male genetic compliment and are far less costly to manufacture and send. In other words, sperm are cheap, eggs are expensive.

Although cheap sperm and compulsory sex are effective tools for propelling the male’s genes into the bodies of future generations, they do so with little regard for the reproductive goals of the female’s genome. Recall from yesterday’s discussion, that the female gender of a species is typically better positioned to be the ‘chooser’ when selecting potential sexual partners; this is in large part due to the above described costs associated with eggs, pregnancy and child rearing. Through selecting only the most fit, well-matched mates, females are able to reap the benefits of their own inclusive fecundity and improve their own reproductive fitness. In opposition, sexual coercion eliminates the female’s choice and adversely impacts her reproductive fitness.

Reproduction drives the process of natural selection. As a consequence of this biological tenet, a decline in a group’s reproductive fitness is countered in one of two ways; extinction or adaptation. Females challenged with deteriorating fitness often undergo morphological and behavioral adaptation to mitigate for the coercive sex practices of males. Just as selection favors the advancing genes of the male, it also favors those traits that enforce the female’s fitness. As weapons in the back-and-forth battle for reproductive victory, the female may brandish many weapons; she may practice avoidance, she might form coalitions with other females or a dominant protective male, she could incite male-male combat, or her physiology could adapt to delay egg deposition or to interfere with the transfer of the coercive male’s sperm. The behavioral and physiological possibilities are nearly endless.

As a case in point, the female ‘agile frog’ (Rana dalmatina) shares a habitat with two-different species of male frogs; the males of her own kind, and those called ‘European common brown frogs’ (Rana temporaria). Both species of male frogs utilize coercive sex as a reproductive tactic, and both will force themselves on the female agile frog. However, if she is subjected to forced amplexus (frog sex) by the male ‘common brown,’ the resultant discharge of expensive eggs will not be profitably fertilized. Because the common brown is a different species, the fusion of his sperm with the agile frog’s ova will not result in the development of viable frog embryos. In this instance, coercive sex results in the female wasting an entire clutch of eggs that could have potentially carried her genes into the future. To mitigate for the loss of eggs by forced sex, the female agile frog will ‘intentionally’ delay egg-laying in hopes of discouraging the male’s incessant reproductive efforts. If after time the male doesn’t seem to loose interest, the female will release a reduced quantity of eggs. Thinking his mission a success, as a response the male will then release his sperm onto the eggs and part ways in pursuit of the next female. By using the somewhat sneaky, though affective, reduced-eggs scheme, the female exerts ‘cryptic choice’ as a method of insuring her reproductive investment and safeguarding her fitness. This case highlights one of many examples in which a female has manipulated a compulsory sex encounter to circumvent a potential decrease in her fitness.


Hettyey, A., Baksay, S., Vági, B., & Hoi, H. (2009). Counterstrategies by female frogs to sexual coercion by heterospecifics Animal Behaviour, 78 (6), 1365-1372 DOI: 10.1016/j.anbehav.2009.09.006



Rana dalmatina Photo by Fabio Turel

From Promiscuous to Palatable, the Making of a Thanksgiving Day Entree

“For the truth the turkey is in comparison a much more respectable bird and withal a true original native of America... he is besides, though a little vain & silly, a bird of courage, and would not hesitate to attack a grenadier of the British guards who should presume to invade his farm yard with a red coat on.” (Benjamin Franklin, 1784)

As demonstrated by the above quote, Benjamin Franklin admired the turkey for its courage, and although the bird may have been somewhat “vain and silly,” in his evaluation it would have served as a better emblem for the newly constituted United States than does the bald eagle, which Franklin would describe in the same transcript as “a bird of bad moral character” and as one that “does not get his living honestly.”

In reflecting on Franklin’s impeachment of the eagle’s morality, it becomes blatantly apparent that his basis for turkey endorsement was not derived from the appraising of the two birds’ sexual fidelity or familial loyalty. If Franklin would have objectively weighed the family values displayed by the bald eagle against those shown by the turkey, he would have undoubtedly praised the eagle for its habit of committing to more-or-less monogamous relationships, and he would have scorned the turkey’s shameless and promiscuous lifestyle.

Despite Franklin’s misinformed backing, the mate-choosing habits of the wild turkey (Meleagris gallopavo) have long been known to diverge from those standards held by the majority of human cultures. Turkeys are sexually dimorphic with the seemingly arrogant males of the species being substantially larger than the females and displaying a showy, red-colored head and neck. Vulgarly hanging from the head of the beastly male are fleshy folds of skin called ‘wattles’ that are composed of erectile tissue that can be engulfed by blood to signal agitation or arousal. Changes in the size and color of wattles can be paraded in combination with raised feathers and loud boisterous calls (i.e. gobble, gobble) to signal potential mates or to intimidate rivals.

Furthermore, in contrast to the typically monogamous bald eagle, turkeys commonly practice polygyny; this means that a single dominant and territorial male will guard a harem of hens. However in some cases, particularly when local populations become over-crowded, small licentious groups of roving males may share a territory – though, of course, they’ll still scrap for female access.

Through mating with multiple females, and guarding those females from rivals, male turkeys, being insensitive to the reproductive aspirations of others, selfishly increase the number of offspring in the population that bear their genes - said differently, their genes experience greater frequency in the gene pool. Genes are also important to the self-indulgent female turkey.

The male’s propensity to mate with multiple females means that he has little time to contribute towards the proper rearing of young, or to providing any type of direct benefit to the female. Not foreseeing any direct benefits herself, the female turkey grants sexual access to those males with the best and brightest displays. In addition to wattles and the red-colored face and neck mentioned above, male turkeys flaunt feathers with red, green, gold and iridescent coloration. The overall brilliance of the male’s colors provides the female with clues as to his health and genetic makeup.

Despite the dominant male’s watch, the female turkey - far from being chaste herself - also strives to maximize the occurrence of her genes in the population. Like the male turkey, she’ll mate with multiple partners. To illustrate the female’s wanton ways even more, consider that in a study conducted by Berkeley’s Alan Krakauer about 45% of turkey nests sampled during a study of the turkey’s genetic reach were found to contain eggs derived from multiple parentages. The genetically sampled broods contained not only eggs from multiple males, they also were found to contain the eggs from multiple females!

Even beyond the female turkey’s flagrant granting of sexual access to multiple males, the California study revealed that females practiced a quasi nest-parasitism during which they would mate with the father of a neighbor hen’s clutch, and then lay the eggs from that clandestine joining in the nest of the neighbor – leaving the ‘cheated spouse’ to care for the young born of her rouge and mischievous mate’s digressions.

In light of Benjamin Franklin’s personification of the turkey as a “respectable bird,” it becomes difficult to comprehend the process that he undertook in achieving his conclusions of 1784… Unless of course in addition to his many other famous accolades, Franklin also happened to be a knowledgeable naturalist. Perhaps he wasn’t making a statement about the turkey’s morals and ethics; maybe he was making a statement about the bird’s fecundity…

Or, as yet another possibility, perhaps the vain, silly and promiscuous turkey holds more commonality with the citizenship than we care to admit…


KRAKAUER, A. (2008). SEXUAL SELECTION AND THE GENETIC MATING SYSTEM OF WILD TURKEYS The Condor, 110 (1), 1-12 DOI: 10.1525/cond.2008.110.1.1

Male Sexual Choice; an Uncommon Occurrence

During last Tuesday’s brief discussion on the sexual selection dynamic that exists between male and female barking frogs (Hyla gratiosa), I mentioned that, as a general rule, the female gender of most species are the “deciders” when it comes to choosing reproductive partners. What was meant by this was that females are more-often-than-not the limiting sex in a population and are thus behaviorally better positioned to choose between competing males during the process of sexual selection. Today, I thought that it may be a good idea to give an example of a species that exhibits a mating system typified by reversed sex-roles; one in which males , as opposed to females, are the limiting reproductive resource.

One of the many unique things about Syngnathidae, the biological Family to which pipefish, sea dragons and seahorses belong, is that its female members lay their eggs directly on the trunk or tail of the male gender. Following the ovipositioning that occurs during copulation, the eggs remain bodily attached to the male where they are subsequently fertilized by his sperm. The male then carries the eggs as they develop, providing protection and in some instances even direct nutritional support via circulatory connections to placenta-like tissues contained within his brood pouch (note: not all Syngnathidae males have true brood pouches, in some species the eggs are attached externally to the male’s body in “sockets” that lack circulatory tie).

Because males take on the responsibility of carrying and protecting the clutch, they’re ultimately accountable for the success of the offspring. Fitness measures, such as the number of viable offspring produced from a mating session, are in part determined by the resources allotted by the male to the embryonic development of the piggy-backing eggs. Of course, another significant factor in the fitness potential of offspring is the health and condition of the female whom is contributing the eggs. It is the female’s health and current condition that the male assesses during the initial stages of mate selection.

Although both mating behavior and organismal reproductive physiology differ greatly between individual species of the Subfamilies Hippocampinae (seahorses) and Syngnathinae (pipefish and sea dragons), the process of precopulatory sexual selection is characterized by a courtship dance in which the female entices the male (sometimes for a period of days) through performing elaborate maneuvers, turns, circles and tail holding. If she appears healthy and passes muster – if she’s got the right moves – the precopulatory dance may be followed by mating as mentioned above; the female deposits eggs into the brooding pouch (or, in some species places the eggs on the male’s body).

Incidentally, if you haven’t witnessed the courtship dance of seahorses or pipefish, you are truly missing out on an extraordinary display!!! Check-out this video from the Monterey Bay Aquarium:







In addition to the fitness potential read from the females’ sophisticated chorography, the Syngnathidae males also inspect the female for other visual cues that may provide indication to as to her health, condition and genetic make up.

To better understand the male’s assessment method, Adam G. Jones, Assistant Professor at Texas A & M, examined the preference of male members of the species Syngnathus typhle (a pipefish) for females displaying indicators of high parasite load. As most folks could imagine, large quantities of parasites can affect the overall health of an animal; these freeloaders tap into their host and drink with delight the vital resources acquired through the labors of their target. Even for the pipefish, large quantities of unsightly parasites observable on the exterior of a potential mate are pointers of poor current health. The parasites are literally unsightly; unsightly because that is precisely how the male Syngnathus typhle weighs the female’s appearance – by sight. Should the male perceive large or numerous dark spots on the female, he is far less likely to choose her as a reproductive partner. This is because the dark spots, the male pipefish assumes, are parasites and may adversely affect the condition of any eggs the female may be carrying; therefore black spotted females represent a risky reproductive investment for the male. However, there is one detail that the pipefish in this experiment weren’t privy to, that is that the dark spots in Jones’s study weren’t parasites at all – they were harmless tattoos.

During a recent visit to Tallahassee, Dr. Adam G. Jones explained that the tattooed pipefish experiment was originally intended as an inquiry into the post-copulatory behaviors of Syngnathus typhle. Knowing in advance that males preferentially mated with females showing low parasite loads, Jones had suspected that males of the species may engage in a cryptic choice behavior in order to reduce impregnation by parasite ridden females. Although this experiment ultimately demonstrated no support for the parasite-to-cryptic choice hypothesis, it did exhibit the possibility for cryptic choice along lines other that parasite load, AND the experiment also provided evidence to two key phenomena. Firstly, the experiment revealed that eggs from larger females had a greater statistical tendency to become viable offspring than those received from smaller females. And secondly, the study showed that the first female to mate with the male deposited a larger quantity of eggs than did those females ovipositing afterwards.

So... The natural history of the Family Syngnathidae demonstrates that male choice does exist in the natural world. Further, Jones’s work has shown that male choice extends beyond the precopulatory selection of female mates and that the behavioral ecology of the pipefish even includes post-copulatory mechanisms of sexual selection.


Partridge, C., Ahnesjö, I., Kvarnemo, C., Mobley, K., Berglund, A., & Jones, A. (2008). The effect of perceived female parasite load on post-copulatory male choice in a sex-role-reversed pipefish Behavioral Ecology and Sociobiology, 63 (3), 345-354 DOI: 10.1007/s00265-008-0668-3

Sexual Selection and Hyla gratiosa: Barking Fast and Barking Long

In regards to sexual reproduction, the selection of potential mates can generally be thought of as functioning along one of four lines; through identifying Good Genes, receiving Direct Benefit, via Sensory Bias and by Fisherian Runaway. However, even though most species have adapted to one of the core strategies listed above, the methods of selection themselves are far from being restrictive. In fact, these strategies of mate choice may operate independently, collectively or in conjunction with other aspects of local ecology and Natural Selection – they’re not by any means exclusive. In a word, the processes under which one chooses a mate can be rather “complex”.

In considering the complexity of this dynamic, evolution and sexual selection have, on the average, placed the female gender in a position to choose between potential male reproductive partners; when it comes to sex, the females are the deciders.

Why?

Well, this is so for a few different reasons. One of which is that females are generally the limiting gender in a population. This means that they ultimately control population numbers and take on the added burdens of producing ova and caring for young – both of which can be taxing to available resources. In addition, females also tend to be fewer in number within a given population, often outnumbered by the males.

So, if the power of mate choice belongs to the female, on what grounds is her selection to be made and what criteria are weighed and measured prior to committing to such a costly reproductive venture?

Certainly, any mate is better than no mate at all, but when the opportunity presents itself wouldn’t it be beneficial to capitalize on the availability of the most virile, successful or healthy male – how to choose?

For Hyla gratiosa, the “barking treefrog,” the female’s choice of mate seems to center on the duration and frequency of the boy’s bark.



I took this H. gratiosa snapshot two weeks ago near Wildwood, Fl

Hyla gratiosa is a rather robust looking treefrog that grows to be somewhere between five and seven centimeters as an adult. Found in the southeastern United States, these guys are easily recognized by their spots, which cover large portions of their back and legs.

Back View of above Specimen

Although generally spending the majority of their time high in the trees, they have been known to venture to the ground during the summer months in efforts to cool off in the shade of herbaceous ground plants. Mating season pushes the males to water where they call, or “bark,” for females. The male’s “bark” during mating season (March through August) is loud and explosive. Often repeated in intervals of a second or two, the duration and frequency of their call has the ability to communicate health and virility to the inquiring female.

You can Listen to a Sample “Bark” from the Smithsonian HERE (at Bottom of Page).

In testing how the female places value on the calls of the male, a couple of researchers from James Madison University recorded and played back the calls to females in order to judge the their response to the stimulus. Basically, they went out and caught females (actively engaged in amplexus), took them to a prepped area, placed them behind blinds, and then played them calls of varying structure. Once the calls had been played, the blind was lifted from the female frog and the researchers watched as she either moved to engage her would be suitor – a sound speaker, or took a non-responsive action.

Going into the experiment, the researchers developed four hypotheses to describe possible ways in which the female may assess the calls:

(1) Single-trait Hypothesis. Females may perceive multiple cues as a single trait, even though researchers may identify them as separate traits.

(2) Amplifier Hypothesis. A trait may not be directly assessed by females but may amplify another trait that is assessed directly, thereby allowing females to better discern differences between males in the assessed trait.

(3) Hierarchical Hypothesis. Females may assess traits in a hierarchical fashion, basing their choice on the higher level trait whenever this trait differs between males and using lower-level traits only when higher-level traits are difficult to discern between males.

(4) Simultaneous Hypothesis. Females may base their choice of mates on multiple traits, combining preferences for individual traits. Preferences for traits may be combined additively.


Following the experiment, the researchers concluded that the females consider both the rate and duration of the call independently, but they show an overall leaning towards high call rates over those of an extended duration. However, this preference only stands true with in certain ranges of acceptability, if the frequency of the male’s call rate falls below a certain threshold, the female will additively consider the duration as well.

Hypothesis 4, the Simultaneous Hypothesis, seems to best describe the female barking frog’s call selecting criteria.

BURKE, E., & MURPHY, C. (2007). How female barking treefrogs, Hyla gratiosa, use multiple call characteristics to select a mate Animal Behaviour, 74 (5), 1463-1472 DOI: 10.1016/j.anbehav.2007.02.017