Sunday, July 22, 2012

Gender part five: Sex determination in some animals

Note: This program first aired on July 21, 2012.

In many species of animal, what makes a male a male and a female a female is tightly controlled by genetic regulation. This makes sense, as species that reproduce sexually rely on having both sexes represented in the population. In other animals though, sex determination is controlled by environmental factors, usually temperature. And if you have been listening to this show long enough, you should be able to guess by now that there is a third system, that is a blend of these two mechanisms.

To begin, regardless of the system used, all of us vertebrates start out with indifferent or bipotential gonads. These could develop into either ovaries or testes. The first mechanism for this differentiation to occur is called Genotypic Sex Determination (or GSD), in other words, the genes you inherit from your parents determine your functional sex. We talked about this quite a bit when we looked at the phenomenon of male nipples. We are familiar with this system because, barring complications that is how it works for most of us mammals. In fact, the group that includes us, the Eutherian Mammals is the most strictly GSD group of animal out there!

The second system is called Temperature Dependent Sex Determination (or TSD), and is favored by many fish and reptiles. In this system, the development of the gonads from the bipotential state is regulated by environmental temperature, during a specific window of early development, called the thermosensitive period. Species utilizing this method have specific temperature thresholds, above, below, or inbetween which the sex determination switches. The third process is the blend. It turns out that some fish and reptiles have a genetically determined sex, but those sex chromosomes can be overridden by environmental temperature, a phenomena and area of research called epigenetics, or the factors that act on genes, turning them on and off. Its these two mechanisms that I want to talk about today, and we can talk about them together because it turns out that the details are the same in both, whether the fish or reptile has sex chromosomes or not.

The primary influence on the sex determination of any non mammalian vertebrate is the ratio of androgens (male hormones like testosterone) to estrogens. The key factor in temperature dependent sex determination seems to be an enzyme called aromatase. It job is to turn androgens into estrogens, thus affecting the critical androgen/estrogen balance. When aromatase is upregulated, androgens are readily converted to estrogen and the result is female. When the aromatase is down regulated, estrogen is not formed and the result is male. In fish that exhibit some form of TSD, the pattern is well established. Temperatures warmer than a critical threshold (that varies by species), down regulate the genes that produce the aromatase enzyme. Warmer water strongly biases the sex ratio in susceptible fish populations towards males. This has been inadvertently demonstrated in some aquaculture operations; the larval fish are kept in artificially warm environments to increase their growth rate, and have turned out to be almost entirely male as well!

Reptiles show much more diversity with TSD. Warm temperature affect lizards and crocodiles differently than it does turtles. In lizards and crocodiles, warm temperatures yield males, like fish. In turtles the opposite seems to be true, warm temperature biases towards females.  This points to multiple pathways for the upregulation and down regulation of aromatase producing and regulating genes.

As a final note from developmental biology, there is strong evidence that even with the plasticity of sex in these organisms, once the developmental window is closed, gender is permanently established. Changing the temperature for the duration of embryonic development will not change the gender of the organism again.

References: Three really good and readable articles with lots of good background information:

Navarro-Martín L, Viñas J, Ribas L, Díaz N, Gutiérrez A, et al. (2011) DNA Methylation of the Gonadal Aromatase (cyp19a) Promoter Is Involved in Temperature-Dependent Sex Ratio Shifts in the European Sea Bass. PLoS Genet 7(12): e1002447. doi:10.1371/journal.pgen.1002447

Pieau C. and Dorizzi M. Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads Journal of Endocrinology June 1 2004 181

Barske, Lindsey and Capel, Blanche Blurring the Edges in Vertebrate Sex Determination Curr Opin Genet Dev. 2008 Dec; 18 (6)

Sunday, July 15, 2012

Gender Part Four: Plants Gone Wild

Note: This show originally aired on July 14, 2012.

We have been spending the past few weeks looking at the biological basis for and variation in gender. This week we continue our look at sexuality in plants.

The vast majority of flowering plants or angiosperms are hermaphroditic, having both male and female reproductive structures on the same plant and usually in the same flower, we discussed those in detail a couple of weeks ago. A small minority of plant species have bucked the trend and evolved to have fully separate sexes, with males and females occurring in entirely different individuals. These polymorphic plants are called dioceious. Gender in dioecious plants is determined genetically and there is, to use the word of one researcher, a “bewildering” level of variability in the sexual structures of dioecious angiosperms.

Plant sexual polymorphism (poly meaning many, morph meaning shape) is a relatively new invention in angiosperms, and this newness is the reason for the variability. Amazingly this form of sex determination is estimated to have evolved over 100 separate times. This means that many many lines of angiosperm plants have, in evolutionary terms, solved the same problem in the same or similar ways. These plants have evolved an XX/XY sex chromosome system, much like ours, but it is relatively new in evolutionary terms, so it is much more complicated and less well resolved than the relatively simple mammalian system. Dioecy (or the state of being dioecious) is not at all the straight forward boy meets girl scenario we humans are used to; in addition to the male meets female system, there are male meets female biased hermaphrodite and female meets male biased hermaphrodite, and mixes of all three as well.  These plants are experimenting wildly with sexual reproduction, beyond the dreams of even the most creative humans. This chaos (and it is chaos, if you don’t believe me, dive into the literature) is a result of the relative youth of the dioecious reproductive system. We’ve already said that angiosperms have the most diverse reproductive structures of any group of organisms. Think of these dioecious outliers as those on the forefront of a new evolutionary wave. Sometimes they succeed, other times they fail. While there is some evidence that this system yields a lower overall reproductive rate, I think it is too soon to judge the results of this evolutionary experiment.

As if all this sexual experimentation weren’t enough, it gets really interesting with the fact that many unisexual plants are diphasic, meaning they change sex, starting as one, ending as another. One reason for this life strategy is environmental stress. A close to home example is the unusual wood and wetland species Jack in the Pulpit, aka Arisaema triphyllum. This is a multi year perennial plant, and when it first emerges, it is non flowering. Then it develops into a male plant. Traditional thinking has it that pollen is a less energy intensive gamete to produce than the larger ovule, hence smaller plants with less resources to devote to gamete production will be male. If the environment is stressful enough, in terms of nutrient levels or space competition, the plant remains male. If it is able to gather enough resources to grow larger, it will switch sexes and present as female in later years. There is evidence that the sex ratio of the plants around it also effects its sex determination. These plants are able to do this because the have a “plastic genotype” that allows them to develop one of a few options depending on the environmental conditions they are presented with in any give growing season. This plasticity, I believe, is a result of the relative youth of this sexual system. This is the wild west of biology, the rules aren’t fully written yet, and these plants are testing the limits of the system, which, as noted above, can lead as easily to failure as to reward.

The other thing we should note, is that if these individuals can change sex, that means that they must have the genetic code for both sexes in their genome, even if they are using a proto version of an X/Y sexual determination system similar to ours. Many vertebrates have no sexual determination genetics, and rely totally on environmental factors for determining gender. As mammals evolved on a branch of the tree of life away from other vertebrates, is it possible that our gender development was as plastic as these plants we now observe? We will consider that in the coming weeks as we continue our exploration of the origins of gender. 


From the Indian Academy of Sciences, a pair of articles in their science education journal Resonance. From 1998, Volume 3 No. 4 R.M. Borge’s Gender in Plants: Why do plants change sex? and Vol. 3 No. 11 R. M. Borges Gender in Plants: More about Why and How Plants Change Sex. Dated, but useful.

Barret, Spencer “The Evolution of Plant Sexual Diversity” Nature Reviews: Genetics April 2002, Vol. 3

Charlesworth, D. “Plant Sex Determination and Sex Chromosomes” Heredity 2002 (88) 94-101 Very technical, good luck with this one. “Gene for sexual switching in melons provides clues to evolution of sex” Website for the University of Pittsburgh Kalisz Lab, a plant research lab.

Saturday, July 7, 2012

Gender 3: Male Nipples and Human Evolution

Note: This program first aired July 7, 2012.

I was asked recently, why men have nipples. As we are currently working our way through the biological issues of gender, I thought this might be a good side track because it takes us from the somewhat silly idea of men’s nipples, to the much deeper and fundamental concepts of evolution and human development.
My initial guess was that men have nipples because nipples are an evolutionary orphan—left over from a time when perhaps both sexes of mammals nursed young.   Another idea was that maybe nipples had some other function in early mammals; regardless, I thought men had them because they once needed them and now don’t, and, like our appendix, they haven’t fully evolved away.
It turns out that, to the best of our knowledge, a small part of my guess was right (which means that large part of it was wrong as well). The part I was right about was the easy part. If an individual has a trait that has a negative impact on its ability to reproduce, that individual’s genes (and the traits they encode for) will disappear from the population. This is the mechanism of natural selection. However, if an individual displays a trait that is neutral to its ability to reproduce, there is no selective pressure that will make that trait disappear.  The bottom line is that once a trait appears in a population, if it isn’t doing any harm, it isn’t likely to disappear. This is the argument for why men still have nipples. While it is possible for men to get breast cancer (not only do they have nipples but mammary tissue as well), it is rare and not affecting the overall reproductive rate of the human population. So, while they are arguably useless, they are likely here to stay.
But this doesn’t really address the primary question, why do they have them in the first place? My thought, that they have them because they once needed them, seems to be all wrong. Almost all male mammals have nipples, and there is no evidence in the geologic record or in current species, that males ever used them for nursing. Mammary tissue originated pre mammal—in a group called synapsids ( first seen about 310 mya—small lizard like animals). They didn’t have nipples per say, but simply nourished their eggs and eventually young with secretions that came out of their skin, through structures related to hair follicles (platypus and other monotremes still lactate this way, picture milk oozing out of the skin of your chest and your infant licking it off you). There is some debate about origin of this tissue, did it arise from sweat glands? sebaceous glands?  or some other related cutaneous gland? Did the secretions nourish live young or as some hypothesize, get absorbed directly through the thin shells of the eggs of these early animals? It is not clear, as this tissue does not fossilize well. But it is clear that lactation predates nipples.
So it seems that the real reason male mammals have nipples is due to the realities of our very early development as embryos. It is commonly said that all human embryos start out “female”; this is an oversimplification that has the ring of urban legend to me, but there is a bit of truth to it. Typically, and in most mammals, individual who carry the XX genotype for their sex chromosomes develop into females, individuals who carry the XY genotype develop into males. All the traits and structures that we think of as human are on the 22 other pairs of chromosomes, including the coding for nipples and mammary tissue. The only difference between males and females is the presence of that Y sex chromosome, and amazingingly, the only thing it does is tell certain cells to make testosterone several weeks into the development of an embryo. That testosterone then tells the sex organ cells to become testes and male genetalia instead of ovaries and female genetalia. Without that testosterone cue, an embryo with an XY genotype will develop in the default mode, as a human who’s development is governed more by estrogen than testosterone, someone we would identify as female. 
Another thing that testosterone pulse does is suppress the development of the mammary tissue (though in humans, not completely). In a few species of mammal, (rats, horses) the testosterone completely suppresses the development of this tissue, and as a result, males of those species have no nipples at all. Again though, nipples on human males don’t seem to cause many problems, so we haven’t evolved such radical measures. In fact, males who experience non typical hormonal patterns or who experience the lower levels of testosterone common in older age can develop more mammary tissue, breasts and even in very rare cases, can lactate.
To recap: Mammals evolved nipples because nipples worked better than sweating milk for feeding young. Men have them because they are in the generic blue print for human being, and there has been no selective pressure to fully get rid of them. And the more we know about the delicate nature of the early development of the human embryo, the more clear it becomes that both native hormones and pollutants that mimic estrogen and testosterone in the body can have a profound effect not only on our health, but on our very identity.

Interesting thoughts from Cecil Adams, the “worlds’ smartest humanbeing” In fact, there are many people blogging about this issue. If you Google “Why do men have nipples?”, you will primarily get blogs as top hits.
“The Mammary Gland and Its Origin During Synapsid Evolution” Olav T. Oftedal,  Journal of Mammary Gland Biology and Neoplasia Vol. 7, No. 3 July 2002

Sunday, July 1, 2012

Gender: Part 2

Note: This program first aired in June 2012.

Today we continue our ongoing discussion of gender and how it relates to biological reproduction and the amazing diversity we see in nature. To review, we know that individuals we call females make ova or eggs, and individuals we call males make sperm, and in humans, this comes with a whole lot of extra baggage (to be fair, many animals exhibit the differences in appearance and behavior called sexual dimorphism, but I believe we are the only species to have come up with misogyny and homophobia among other things).

When it comes to reproductive equipment, flowering plants, technically called angiosperms, have all other groups of organisms beat. As a group, angiosperms have the highest variety of reproductive structures on Earth. In this group, the most common sexual form is the hermaphrodite, meaning both female and male components are found in the same flower. These flowers can also be referred to as bisexual, and are botanically classified as “perfect”. It is thought that all angiosperms evolved from a hermaphroditic ancestor, and single sex, non hermaphroditic strategies evolved later. This is why 75 to 85% of angiosperms are hermaphrodites.

What are the benefits of being a hermaphroditic plant? The one that jumps to mind initially is that if there are no other potential mates around, you can fertilize your self. In theory this works, but most plants actually go to great lengths to avoid this phenomenon (called “selfing”).  Like interbreeding in royal families, selfing tends to bring out genetic weaknesses over several generations. Think of selfing as a last chance scenario, especially for annual plants, who live only one growing season and “winter over” in seed form. If the plant doesn’t get to mate with anyone else, at least it can sustain itself over the winter as a seed generated from a self fertilization; ideally in not too many generations in a row.  

Another way that hermaphrodism increases an individual’s chances of mating is in a low density potential mate situation; a less extreme version of what we just talked about. If there are very few potential mates around, what happens if they are all male? Or all female? They aren’t the isolated individuals of the former scenario but they still can’t mate successfully in a single sex group. Hermaphrodism in plants ensures both sexes are represented, even in a low density population.

Yet another benefit of hermaphrodism in plants is that it extends their mating season. Hermaphrodites can functionally bias their flowers towards one sex or the other for various reasons. While the flower will have both male and female sexual structures (the androecium and gynecium respectively), they may not be functional at the same time. For example the male may mature first, and produce pollen. Later the female parts will mature, ready to accept pollen from a separate individual. The plant has then essentially doubled the amount of time it is spreading and mixing its DNA, and has eliminated the chance of selfing as well.

The bet hedging, flowering species of the plant kingdom have clearly benefited from utilizing both genders simultaneously for millions of years, yielding extraordinary biodiversity and resilience. And with all of our ideas about gender and value, sexuality and stereotypes, most of us just see the flower.


From the Indian Academy of Sciences, a pair of articles in their science education journal Resonance. From 1998, Volume 3 No. 4 R.M. Borge’s Gender in Plants: Why do plants change sex? and Vol. 3 No. 11 R. M. Borges Gender in Plants: More about Why and How Plants Change Sex. Dated, but useful.

University of Oxford’s Science Blog features a conversation from March 2009, with Dr. John Pannell of the Oxford Dept. of Plant Sciences

Dr. Spencer Barrett’s “The evolution of plant sexual diversity” is lengthy and quite technical, but dedicated readers may find much to ponder. April 2002, Vol. 3