Not Exactly Rocket Science

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For humans and most other mammals, sex is a question is chromosomes. Two X chromsomes makes us female while an X and a Y makes us male. Birds use a similar but reversed system, where males are ZZ and females are ZW. But for reptiles, including crocodiles, turtles and many lizards, sex is determined not by genes, but by temperature. 

In crocodiles, males hatch from eggs incubated at cooler temperatures while warmer conditions produce females. In turtles, it’s the other way around, and lizards use a variety of criteria including some very complicated combinations of genes, temperature and even size of egg.

But what did extinct reptiles do? It’s not exactly easy to tell for genes and temperature don’t fossilise. However, fossils can tell us about how such animals reproduced. For example, we know that three groups of marine reptiles - the serpentine mosasaurs, the dolphin-shaped ichthyosaurs, and the long-necked, paddle-flippered sauropterygians – gave birth to live young through a series of stunning fossils of pregnant females, and even one case of a birth in progress (see below). Around 20% of living reptiles (excluding birds) do the same and the ability probably evolved at least 100 times in lizards and snakes alone.

Chris Organ from Harvard University thinks that, in all three lineages of marine reptiles, the evolution of genetic sex determination preceded the evolution of live births. By studying the reproductive styles and sex-determining methods of 94 species of amniotes (mammals, birds and reptiles), he showed that the two traits often co-evolve. Live birth almost always depends on first having a gene-based method of assigning sex, while egg-layers can use either chromosomes or temperature.

Organ suggests that these important changes were instrumental for the success of these prehistoric swimmers, allowing them spread throughout the open oceans, where temperatures can’t be relied on to determine sex. And without the need to return to land to lay their eggs, they were free to live permanently at sea and evolve more extreme physical adaptations to an aquatic life, including paddle-like limbs, back fins, streamlined bodies and fluked tails.

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Among the amniotes, every group that lives permanently in the sea gives birth to live young and relies on sex chromsomes to set the males apart from females. For whales and manatees, that’s hardly surprising, for all other mammals do the same but it’s notable that sea snakes use the same system too and they are the only permanent marine reptile. Others, like turtles, saltwater crocodiles and marine iguanas, are either tourists in the oceans or need to lay eggs on land.

Organ plugged all the data from his 94 living species into a mathematical model that could predict the likelihood that other species determined their sexes through genetic means. The model correctly predicted the systems used by animals such as the extinct horse Propalaeotherium, which also left behind fossils of pregnant females; the European asp, a snake that gives birth to live young; and the southern water skink, one of only two animals that uses temperature to determine sex but gives birth to live young.

i-d8772b77112a0df2b14b9084093b758b-Phylogeny-thumb-200x106-19057.jpgConfident in his model, Organ used it on ten extinct species and it predicted with over 90% certainty that ichthyosaurs and sauropterygians used genetic sex-determination and over 99% certainty that mosasaurs did so.

Organ speculates that GSD evolved in the land-based or amphibious ancestors of all three groups, before they made the move to water. Their ability to set the sex of their offspring without having to worry about incubation temperatures freed them to diversify in the ocean environment.

Each event was a major one, sending a new wave of top predators into the oceans to compete with each other, and with existing hunters like sharks. Some of these newcomers did very well and grew to giant size – the ichthyosaur Shonisaurus, for example, was over 20 metres long.

Reference: Nature 10.1038/nature08350

Images: Reconstructions Arthur Weasley, Haplochromis

More on temperature sex-determination:

Comments

  1. #1 Michael Dybevick
    September 16, 2009

    Do I understand correctly? You cannot tell from a crocodile DNA sample whether the supplier of the sample is male or female?

  2. #2 Nathan Myers
    September 16, 2009

    Michael: Do you count methylation among measurable details of your DNA sample?

  3. #3 Michael Dybevick
    September 16, 2009

    I don’t know enough to answer that. They didn’t cover that in engineering school. I will educate myself on methylation and restate if necessary. Thanks for the clue.

  4. #4 Ed Snack
    September 16, 2009

    I may be wrong, but I believe that there are indeed distinguishable Male and Female crocodiles as adults. Only those who are female can lay eggs. Those eggs develop into male or female animals based on the temperature of incubation. Thus there are genetic differences between male and female, but these are not used to determine the sex of each egg. After all, crocodiles don’t auto-fertilize, they mate to produce viable offspring.

    Infelicitous phrasing by Ed I suspect.

  5. #5 Nathan Myers
    September 17, 2009

    Michael: Methylation is especially amazing. Biologists have known about it for decades, but because they’re not engineers (and they’re insane) they didn’t think it was interesting enough to mention to anybody. Get this: Each spot on the DNA chain where there’s a C (cytosine) can have a methyl tag stuck on, like a post-it note. This tag is noted by enzymes that operate on DNA (e.g. in deciding whether to express a gene) and copied when the DNA is copied. There are enzymes for sticking on methyls and enzymes for taking them off, and enzymes to move them around. Methylation is how cells know they they should be doing bony things, or skinny things, or nervy things.

    Apparently whether a crocodile is male or female depends on where the methyls have been stuck on in the relevant batch of cells.

  6. #6 Jay Kehl
    September 17, 2009

    Nathan: Methylation might control sex-determination, but given methylation controls *all* gene regulation that’s not really saying much.

    My quick web-search suggests it’s more like temperature->gene expression->enzymes(e.g. aromatase)->(testosterone|estrogen)->sex-development for quite a few reptiles…

  7. #7 Nathan Myers
    September 17, 2009

    Jay: A large majority of the gene regulation in all organisms is controlled by whether the gene in question is physically present in the organism. Methylation controls the rest.

  8. #8 Dunbar
    September 17, 2009

    Nathan, your last comment made little sense. You said that “gene regulation in all organisms is controlled by whether the gene in question is physically present in the organism”. I have no clue what that means exactly. Moreover, there are many other gene regulatory mechanisms that are well recognised and well characterised, such as transcription factors and post-transcriptional regulation such as siRNA. That is, methylation assuredly does not control gene regulation to the extent that you claimed. For instance, methylation in bacteria does not regulate genes.

  9. #9 Nathan Myers
    September 17, 2009

    Dunbar: My comment was in response to Jay’s “given methylation controls all gene regulation“. I defy you to express a gene you don’t have. My “the rest” was echoing Jay’s corresponding exaggeration.

  10. #10 Michael Dybevick
    September 18, 2009

    So do I have this right?

    A DNA sample from a newly deposited egg will have little or no indication as to the sex of the future adult. After some time in incubation however, a DNA sample from the same egg will show some methylation of the DNA, which may or may not be directly “readable” but will steer development toward one sex or the other.

    Does methylation have anything to do with pleiotropy, like it is discussed here?

    http://scienceblogs.com/pharyngula/2009/09/isnt_pleiotropy_handy.php

    This makes the genetic code sound less like the pristine and deterministic set of four buildng block combinations I learned in high school and more like a pile of 15 year old computer code that has survived its original authors and is being maintained by an ever expanding set of wrappers that control what parts actually get called and maybe touch up some of the results as they bubble up.

    Methylation is the Windows front end on the legacy green screen app.

  11. #11 Nathan Myers
    September 18, 2009

    Michael: Exactly so, except there was never anything there but touch-ups. That feeling you get, with Windows code, of astonishment that it can ever work at all, is continuous and indefinitely recursive in biology.

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