The Ugly Butterfly Gets The Girl

Biology concepts – fluctuating asymmetry, mate selection, honest signal, directional asymmetry

Facial symmetry supposedly plays a role

in physical beauty, but may represent

developmental stability, an ability to resist

disease, and of genetic strength.

The reasons that one human picks another as a mate are unique to the individual; personal history, social mores, and biology all play a role. No matter what e-Harmony or Match.com tell you, a complete understanding of how two people match for life is truly unknowable. Do opposites attract in a meeting of the minds? Is it all about chemistry and the way someone smells? Do big muscles and child-bearing hips play a central role?

Bilateral facial symmetry is thought to play a role in what people think is pretty, and pretty plays a role in mate selection. Why? Because symmetry implies a stable embryologic development and good genes – or maybe not. As Shakespeare wrote in A Midsummer Night’s Dream, “The course of true love never did run smooth;” it applies here.

Bilateral asymmetry takes three forms; fluctuating asymmetry, directional asymmetry, or antisymmetry. In terms of humans and pretty faces, it’s fluctuating asymmetry that we’re talking about.

Take a sharpie and draw a line from the top of your head down to the split in your legs – no, don’t really do it, this is just a thought demonstration. If you were to measure the distance from that midline to the same point on each of your eyes or ears or any body part, the length on the right will be close to the length on the left, but probably not exactly the same.

The same would be true if you measure the heights from the floor to the bottom of some body part like your eyes, or if you measure the length of fingers on each hand. The differences represent fluctuating asymmetry (FA), and your neighbor’s will be different from your own – we say that FA is what gives faces character.

President Lincoln had a defect called facial

micronesia. The left side of his face was much

smaller than the right. The middle image

above is his face. The left image is his right

side flipped and placed against his right side.

The right image is made from two left halves of

his face. Everyone’s right face and left face

look different; his is just a greater than average

difference.

Your body has a plan that determines where each eye or ear will go, and in a perfect world, it would be exactly the same spot on each side of the midline. But your genes don’t control the implementation of the body plan – what you end up with in terms of symmetry is based on the environment in the womb and how well your genetics can compensate for it.

In other words, the more instability there is in the developmental environment, the higher the FA could be. What might stop fluctuating asymmetry from becoming large? Some scientists believe it to be good genes. The instability in the womb could come from disease, toxins, parasites, drugs, stress… who know how many things might be involved.

But if your immune system is strong – partly a genetic trait, then perhaps you could control in utero diseases and FA could be kept to a minimum. For just about any stressor you can imagine, there could be a genetic response that, if healthy and strong, could minimize the damage from the stressor.

In terms of picking a mate, unconsciously sensing low levels of FA suggests to your primitive brain that the genes of this individual might be more adapted to the environment - good potential parent. And that’s all that really matters to an organism at the basal level – having strong offspring.

A 2005 study in Jamaican teenagers showed that

those teens that were rated as better dancers had

less FA. As always, cause and effect is elusive.

Did symmetry make them better dancers, or
 were they perceived as better dancers because

they were more symmetric? Regardless, good

dancers do have a reproductive advantage.

A 2014 study concluded that males with less body FA are stronger with respect to hand grip. They suggest that since strength is a quality used in mate selection and male competition, increased strength may be one reason why symmetric males are considered better mates – they win out in more intra- and intersexual competitions (they're more appealing and win more fights). Just how symmetry brings strength was not discussed. Together, symmetries are considered to reflect fitness, so in terms of non-verbal communication to potential mates, they are considered honest signals, traits that represent truth about the possessor.

A 2012 study in rhesus monkeys built upon the result of a previous experiment in that macaques stare at symmetric faces longer than faces with higher FA. This was supposed to mean that they preferred the symmetric faces. And there is evidence to suggest that our brain does find symmetry in objects, scenes, and art more pleasurable.

So the 2012 study measured both the FA and the health of female macaques. Using veterinary health standards, number of wounds and weight gain over first four years of life, the females with less FA had the best health. This supported the hypothesis that better genes result in better health.

To my mind, there is also the possibility that less FA leads to being treated better within the group, which results in better overall health. Since primates prefer symmetric images, a symmetric face (the seat of social communication) might result in more food offered, fewer fights, and/or less stress – and therefore a better overall health rating. This idea suggests that better health is a result of symmetry, not the other way around. In this case, wouldn’t facial symmetry be a dishonest signal? Is anyone studying this?

There is evidence that supports this notion, or at least lessens the strength of the symmetry and fitness hypothesis. A 2015 study in Senegal found no link between malaria rates and FA in teenagers. This suggests that FA doesn’t predispose to malaria (lack of fitness meaning higher susceptibility), and that malaria does not increase FA.

FA isn’t just a measure of “beauty.” A 2013 study

showed that urban lizards display more FA than

rural lizards. The hypothesis is that urban living

increases exposure to stress and pollutants, and

this manifests as increased FA. If true, tracking FA

could be used a measure of pollution and its effect

on wildlife.

Likewise, a 2011 paper showed that poverty was linked to increased FA. This is a touchy subject. The study found higher FA in young males from the poverty stricken sections of Ankara, Turkey. Does this mean that the stress of poverty destabilized the developmental environment of males, either in utero or afterward? Or does it mean that the stress of poverty increases FA? Does it mean that people with weaker genomes end up in poverty? Would people with better genes be more likely to resist the FA that might result from poverty-induced stress?  I leave it to you to argue that one out.

One could make a strong argument that humans have invented their way out of needing to rely on finding mates with low FA. Our technology, medicine, and brains have helped us to overcome our environment (sometimes to our detriment) so that a different set of traits might be more telling as to the fitness of partners. Intelligence, puzzle solving, emotional quotient and even tendency to maintain monogamy might be more desirable today. But the instinct to look for low FA has been stuck in our brain by evolution and it doesn’t care about logic.

Why do I bring up emotional quotient and monogamy? Some studies reviewed in 2010 show that lower FA in human males and females correlates with more extramarital or extra-significant other affairs (called extra pair coupling, EPC). Males with more symmetrical bodies sought out more EPC and females who engaged in EPC were more likely to seek out men with low FA. Not a great commercial for symmetry.

It isn’t just humans that sense symmetry and use it for mate selection. The primate studies above show that it extends to macaques, but birds do it was well (as do probably animals in other phyla). Peahens look for symmetric tails in peacocks and barn swallow females look for makes with symmetric and long tail feathers.

The left butterfly is paler; it's a territorial male. The

right speckled wood butterfly male is non-territorial.

 He flits from area to area looking for the females not

in a sun spot. If he competes with a territorial male –

he always loses. He has more FA than a territorial

male, but no directional asymmetry.

Everything we have said above states that animals look for symmetry in mates, but there are exceptions. The speckled wood butterfly (Pararge aegeria) is a great example. The biggest exception of all is that the females prefer asymmetry – a bit.

This European and North African butterfly has two male morphs. One is territorial, it's a paler color and has fewer spots on it’s wings. The other morph is darker, has dark spots and is non-territorial. The territory they fight over is a sunny spot where the light comes through the forest canopy.

Females are more likely to be in the sun, so territorial males will fight over a sunny spot territory. The contest between males is aerial; combinations of acrobatics and duration determine the winner – except when the territory is being defended. Sound a bit confusing?

In 1978, a paper addressed this. The author found that the defender of a territory ALWAYS won the flying competition. It’s a weird way of determining who will probably mate more often if they already know the outcome. A non-territorial male will compete, but will always lose.

The only time the competition isn’t rigged for the defender is when the spot has no owner, or both males believe it to be their territory. Then the flight contest is much longer and more intricate. This is where the asymmetry comes in.

The territorial speckled wood butterfly males seek

out sun shafts in the forest. This is where the girls

will be, but it also makes them better at the flying

competition. Their time in the sun warms them up

according to a 1998 paper. Being ectotherms, warmth

means they will fly with more energy and win

more contests.

Males have some FA in their wings, but females have much more. What might be limiting the asymmetry in the males? The flying competition. A 1999 study looked at the asymmetry in the wings and noted that those males that had some asymmetry, but not too much, turned in the air faster and could stay aloft longer in a downward spiral maneuver – the main competitive move for males in an honest contest for a territory.

If asymmetry helps win the territory when it is up for grabs, then it will provide more contact with females. This means that this asymmetric (uglier?) male will have more reproductive success and his version of asymmetry will be passed on, if it's genetic.

FA is generally not considered genetic, but directional asymmetry is. The fluctuating asymmetry in the males is low, but the asymmetry that helps win competitions seems to be directional, so it could be genetic. The asymmetry that helps flying is slight, so it is a middling asymmetry that should be passed on.  The fact that females and non-territorial males have more asymmetry suggests that keeping asymmetry low is energetically costly (think about it).

Directional asymmetry in the wings has a functional advantage so it is worth the cost, whereas FA is allowed to get larger. It just so happens that directional asymmetry and antisymmetry are our subjects for next week.

Wade, T. (2010). The Relationships between Symmetry and Attractiveness and Mating Relevant Decisions and Behavior: A Review Symmetry, 2 (2), 1081-1098 DOI: 10.3390/sym2021081

Little, A., Paukner, A., Woodward, R., & Suomi, S. (2012). Facial asymmetry is negatively related to condition in female macaque monkeys Behavioral Ecology and Sociobiology, 66 (9), 1311-1318 DOI: 10.1007/s00265-012-1386-4

Fink, B., Weege, B., Manning, J., & Trivers, R. (2014). Body symmetry and physical strength in human males American Journal of Human Biology, 26 (5), 697-700 DOI: 10.1002/ajhb.22584

Thomas F, Doyon J, Elguero E, Dujardin JP, Brodeur J, Roucher C, Robert V, Missé D, Raymond M, & Trape JF (2015). Plasmodium infections and fluctuating asymmetry among children and teenagers from Senegal. Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases, 32, 97-101 PMID: 25725158

Lazić, M., Kaliontzopoulou, A., Carretero, M., & Crnobrnja-Isailović, J. (2013). Lizards from Urban Areas Are More Asymmetric: Using Fluctuating Asymmetry to Evaluate Environmental Disturbance PLoS ONE, 8 (12) DOI: 10.1371/journal.pone.0084190

Ozener B (2011). Does urban poverty increase body fluctuating asymmetry? Collegium antropologicum, 35 (4), 1001-5 PMID: 22397230

For more information or classroom activities, see:

Fluctuating asymmetry -

http://www.animalbehavioronline.com/fa.html

http://www.uvm.edu/~biology/Classes/102/PDF/Asymmetry.pdf

http://www.mdpi.com/journal/symmetry/special_issues/fluctuating_asymmetry

http://www.philo-online.com/TEXTES/SWADDLE%20John%20P.%20Fluactuating%20asymmetrie.pdf

http://www.biology.ualberta.ca/palmer/asym/asymmetry.htm

http://www.biology.ualberta.ca/palmer/pubs/92P+S/Palmer92_ActZoFenn_FA.pdf

Half Male, Half Female, Completely Weird

Biology concepts – sex determination system, gynandromorphs, non-disjunction, mitosis, bilateral symmetry, chimera, mosaicism

Ardhanarishvara is just form of the god Shiva.

As a male, he is considered the ultimate man,

James Garner mixed with a little Steve McQueen.

Parvati, his wife, wanted to share his experiences,

so he became half her. That’s one

progressive marriage.

In the Hindu faith, Shiva is the destroyer. Anything that has a beginning must have and end, so as Brahma made the world Shiva must destroy it so that it can be remade. On a more positive note, Shiva is also the god of change, making people better versions of themselves by destroying the ego and bad habits.

Shiva is male and celibate, although he has a female consort named Parvati (aka. Shakti, Devi, or Uma). There is also a deity called Ardhanarishvara, which is a half male/half female representation of Shiva + Parvati. The icon is found in most temples to Shiva, but this deity rarely has temples dedicated to him/herself.

Evolution chose to go the other way with nature. In more complex animals, the sexes are separated and join energies to reproduce. In biological terms, it’s a matter of increasing genetic diversity, the source of mutations and drift for natural selection.

However, like Ardhanarishvara, nature sometimes gives us a mixture; a normally two sex species will produce an individual that is part male and part female. And sometimes they're exactly half and half. This is going to take some explaining.

Every once in a while, some embryos have a mistake in mitosis. When the chromosomes line up for random assortment and portioning into the daughter cells, things can go wrong. Once in a while, two chromatids (the two copies of a replicated chromosome) may get pulled into the same daughter cell instead pulled apart with one going to each daughter (called a non-disjunction event).

This produces one cell with too many copies of that chromosome, and one cell with too few. Both outcomes can cause problems. Sometimes, the problem is just cosmetic; sometimes it’s deadly.

Gene loss can come from losing a part of one

chromosome, or you might lose the whole

chromosome (monosomy). It could occur from a

non-disjunction or from some toxic event. A 2015

study shows that smoking can cause a loss of the Y

chromosome in some cells. This makes men more

at risk for some cancers due to smoking (those

outside the lung).  Still want a cigarette?

On the other hand, on very rare occasions a chromosome will be lost during mitosis (chromosome loss event). It ends up next to that sock you can’t find in the washer. Who knows where it is – it just ain’t where it ought to be. One daughter cell has the right number of chromosomes and the other has one too few. Again, the consequences can range from small to really big.

A third possibility exists, where a mutation occurs in one chromatid after replication, so that even if the mitosis is normal (which it almost always is) one daughter will have a mutation (one normal and one mutated gene on the two chromosomes of the same type) and the other won’t (two normal genes on two normal chromosomes).

From then on, every time the daughter cells divide they increase the number of mutated and normal cells. The animal, if it survives to be born, will be a chimera (a mixture of two genotypes). The original chimera was a Greek mythical figure made from the parts of many animals and which breathed fire. It was a half-brother to the Hydra and Cerberus, the three-headed dog. Here it means something less menacing, but just as interesting.

Special circumstances can bring special kinds of chimeras. Which type is formed depends on when the mutation, non-disjunction, or chromosome loss occurs. In some animals, the first cell division after fertilization establishes right and left halves of the animal. Every progeny cell from one of the first daughters will be one side of the body, while every cell coming from the other original daughter will be on the other half of the animal.

The lobster on the top is a mosaic, the mutation

which changed the pigment occurred at a point when

some mutated and some non-mutated cells were on

each bilateral half of the embryo, so there are patches

of each. The bottom version had a mutation that

occurred precisely as the embryo was determining

right and left sides.

If the chromosome change or gene mutation occurs at this point, then exactly one half of the animal will have the change and the other half won’t. This is a bilateral chimera. On the other hand, of the mutation/change occurs at some other point, the there will be patches of one type of cell and patches of the other. This is called a mosaic (see picture to the right).

A 2013 review talks about mutations in different populations of cells and the right left isolation of some mutations. The authors point out that in bilateral chimeras, it is easy to study subtle effects of the gene mutation – one half displays the mutation, and the other half doesn’t. A single animal (could be a person) can serve as the experimental model AND  the control.

For example, in fruit flies (Drosophila melanogaster) the males are XY and the females are XX. If there was chromosome loss early in development, with a single X lost in one daughter cell, there will be XX daughter cells and X (called X0) daughter cells. X0 cells are male because the primary sex determining is located on the X chromosome. In this case just described, the XX cells are female and the X0 cells are male, in the same animal!

This animal would be a gynandromorph chimera. The word is very telling, since gyno = female and andro = male. This is different from a hermaphrodite. The hermaphroditic animal has two sets of genitalia, one female and one male (whether they work or not is another question). In a gynandromorph, the two cell populations of the entire animal show different sex chromosomes.

The patterning on the thorax and abdomen is a bit

hard to see, but the eyes are easily picked out on the

gynandromorphic fruit fly. The pigment genes are

on the sex chromosome.

Gynandromorphs are extremely rare. In fact, they have been demonstrated in only two groups, but this is preliminary. Remember how we talked about animal sexual dimorphism a few weeks ago? Well, it’s only in sexual dimorphic animal species that you would actually notice gynandromorphs (of course, there are exceptions).  

Birds and arthropods are the two animal groups where we have seen gynandromorphs. We gave the example of fruit flies above. You can check out the picture of one to the left. This is specific example of gynandromorph, a bilateral gynandromorph. The left side is female and the right half is male.

In different systems of embryonic development, chimeras can develop side to side (bilateral), front to back (polar), or corner to corner (oblique). This is if the mutation or change in chromosome or gene number takes place at exactly the right mitotic event that divides an animal. If it is any of the other time, the animal will be a mosaic.

In the bilateral gynandromorphic fruit fly above, the color of the eyes is different on each side, as is the body coloring and some other characteristics. This is because the secondary sex characteristics that determine sexual dimorphism are linked to the sex chromosomes.

Spiders have funky sex-determination systems, but

they can still have gynandromorphs. The coloring is

different, but there’s more. It is hard to see, but only

the male side (purplish) has the palp organ growing

on the second appendage for the transfer of

reproductive cells. Image via: spider silk stockings

But wait – normal male and female fruit flies both have red eyes. Here one is red but the other is white. That’s because the gene for eye color and body color pattern in fruit flies is carried on the X chromosome too. If the loss of a chromosome leaves that side of the body with only one X (XO male) and the X it has carries the recessive white eye color gene, then that eye will be white. The other half (XX female) might have dominant red and recessive white eye genes on its two X chromosomes, so that eye would be red.

Is a bilateral difference in coloration enough to call an animal bilaterally asymmetric? They are phenotypically (how they look outwardly) asymmetric, but you cut them in half the silhouettes would be exactly the same (body plan is still symmetric). You can argue amongst yourselves as to what makes an animal bilaterally asymmetric.

Gynandromorphs in vertebrates are extremely rare. The reason for this is that sex characteristics aren’t only controlled by genes on the sex chromosomes. They are also under the control of hormones. But gynandromorphy does occur in birds – they’re vertebrates, but different somehow. No one is quite sure why gynandromorphs are possible for them.

It could be that the mistake comes when multiple male reproductive cells are successful in fertilizing one egg cell. When the fertilized egg cell divides, the daughters would probably be asymmetric with respect to sex chromosomes. Since the sex chromosomes control the production of the reproductive organs, and those organs then make the hormones, you can see how the two are linked.

The gynandromorphic chicken on the left is more a

mosaic than completely bilateral. The male side (your

right) has bigger breast muscle, leg spur, bigger wattle

and white feathers (see the sporadic darker feathers –

it’s a mosaic). A 2010 study showed that if you

transplanted male cells on to the female side, they

retained their secondary sex characteristics –hormones

ain’t everything. The cardinal on the right is striking –

the perfect Ball State University mascot.

The key is in determining which of the sexually dimorphic traits are under strictly genetic control and which are under hormonal control. A study in a gynandromorphic finch in 2003 showed that not everything is hormones. The brains of the males and females are different (in part this determines the song the bird sings) and gynandromorphic finches have brains that are half male and half female in structure. Even with hormones that circulate throughout the body, the brains are still different. The finch of the study sang a male song and mated with a female (no offspring). The male behaviors were controlled by the male part of the brain.

A very rare gynandromorphic cardinal was spotted and subsequently studied for 40 days from afar. The paper reporting this study stated that the bird never sang, never drew the attention of other birds, and never mated. It was a complete loner. But could he/she mate?

Most female birds have one horn of the uterus (left side) that is functional while the other is small and nonfunctional (makes them lighter for flight). Male birds usually have one long testis that is functional, the right one. Since neither male or female birds (most of them) have external reproductive organs, then a gynandromorph bird where the left half is female and the right half is male might actually have a shot at being fertile. It would all depend on how the hormone battle played out.

However, gynandromorphs in mammals don’t happen. The sex hormones control too much of the systems and flow throughout entire body, so you can’t really keep secondary sex characteristics limited to a geographically determined set of cells, even if the sex chromosomes are different in the cells.

Butterflies show sexual dichromatism (different colors

in males and females) and well as different morphologies

of wing (shapes), The gynandromorphs display both, so

they are truly bilaterally asymmetric. Butterflies have an

XX and XY (XO) sex determination system like fruitflies,

except here the XX’s are male.

But there are some characteristics that are hormone independent. Some sex characteristics are set BEFORE the sex determining genes on the sex chromosomes are turned on (reviewed here). The sex characteristic is a default, and therefore is seen both males and females despite later hormone differences. That’s why men have nipples. Nippled is the default state, no nipples isn’t possible. And three nipples is just weird.

The example I like to give for the bilateral gynandromorphy that shows true bilateral asymmetry is butterflies. The male and female often have different coloration and wing shape. This makes them sexually dichromatic within one animal but also bilaterally asymmetric.

Next week we’ll back to the butterflies and asymmetry. There’s one butterfly who is attractive to the girls precisely because he’s asymmetric.

Renfree, M., Chew, K., & Shaw, G. (2014). Hormone-Independent Pathways of Sexual Differentiation Sexual Development, 8 (5), 327-336 DOI: 10.1159/000358447

Dumanski, J., Rasi, C., Lonn, M., Davies, H., Ingelsson, M., Giedraitis, V., Lannfelt, L., Magnusson, P., Lindgren, C., Morris, A., Cesarini, D., Johannesson, M., Tiensuu Janson, E., Lind, L., Pedersen, N., Ingelsson, E., & Forsberg, L. (2014). Smoking is associated with mosaic loss of chromosome Y Science, 347 (6217), 81-83 DOI: 10.1126/science.1262092

Zhao, D., McBride, D., Nandi, S., McQueen, H., McGrew, M., Hocking, P., Lewis, P., Sang, H., & Clinton, M. (2010). Somatic sex identity is cell autonomous in the chicken Nature, 464 (7286), 237-242 DOI: 10.1038/nature08852

Peer, B., & Motz, R. (2014). Observations of a Bilateral Gynandromorph Northern Cardinal ( ) The Wilson Journal of Ornithology, 126 (4), 778-781 DOI: 10.1676/14-025.1

Ma, K. (2013). Embryonic left-right separation mechanism allows confinement of mutation-induced phenotypes to one lateral body half of bilaterians American Journal of Medical Genetics Part A, 161 (12), 3095-3114 DOI: 10.1002/ajmg.a.36188

For more information or classroom activities, see:

Sex-determination system –

http://www.ncbi.nlm.nih.gov/books/NBK9967/

http://www.nature.com/scitable/topicpage/the-sex-of-offspring-is-determined-by-6524953

http://ed.ted.com/lessons/sex-determination-more-complicated-than-you-thought

http://biology.tutorvista.com/cell/sex-determination.html

https://genetics.knoji.com/5-types-of-sex-determination-in-animals/

http://www.shmoop.com/genetics/sex-determination-linked-traits.html

http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.1001899

http://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=18&ved=0CEwQFjAHOAo&url=http%3A%2F%2Fwww.life.illinois.edu%2Fib%2F201%2Flectures%2FSexChrom%26SexDet.pdf&ei=yf8aVfaYKtXpoATIoYKYCg&usg=AFQjCNGsxyoi8qMIRx3NozWnA_isAHAtpQ&sig2=HRjU4JyeOOscWwU5pGv8Dw

http://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=20&ved=0CFwQFjAJOAo&url=http%3A%2F%2Fwww.bio.brandeis.edu%2Fclasses%2Fheredity%2FLecture%2520Powerpoints%2Fchapter7-2.pdf&ei=yf8aVfaYKtXpoATIoYKYCg&usg=AFQjCNF0Lt3s05MtPEjWn1FNVBfNnD7_Iw&sig2=pL5chNP_26THE4F3FkoWJQ

http://www.techtimes.com/articles/2397/20140103/scientists-decode-honeybee-sex-determination-system.htm

Gynandromorphy -

http://www.daltonstate.edu/galeps/Gynandromorphs.htm

http://www.iflscience.com/plants-and-animals/bilateral-gynandromorphs-animals-are-quite-literally-half-male-and-half-female

http://www.slate.com/articles/health_and_science/science/2015/01/half_male_half_female_animals_how_gynandromorphs_occur_in_nature_video.html

https://amasianv.wordpress.com/2012/05/16/its-a-male-its-a-female-no-its-a-gynandromorph/

http://www.livescience.com/14209-gynandromorph-birds-genetic-anomaly-sex-identity.html

https://www.youtube.com/watch?v=oAdTyk_fbBM

http://news.nationalgeographic.com/news/2010/03/100315-half-male-half-female-chickens/

http://www.fromquarkstoquasars.com/beautiful-genetics-bilateral-gynandromorphs/