Thursday, August 11, 2011

Even You Can Create a New Species - The Curious Case of Polyploidy

There are currently 1.7 million named species of plants, animals and algae on this planet.  This does not include the vast array of bacteria and other such single-celled creatures.  And those are only the ones we know about – based on rates of discovery, the National Science Foundation estimates that we have only described 10% of the world’s true diversity.  Most of these organisms will likely be small or marine, but not all; twenty-five species of primates have been discovered since 2000 alone.  And then this diversity really only scrapes the surface of the total diversity that has ever existed, with a mind-boggling number of plant and animal species known only from the fossil record.

Theodosius Dobzhansky, in Genetics and the Origin of Species (1937), presents, in chapters 7-9, an introductory treatment on the topic of speciation.  He brings genetics and natural selection and various observations together to provide a compelling account of how new species are formed.  This would be the groundwork used by Enrst Mayr, who would develop the modern Biological Species Concept.

Dobzhansky was faced with a tough challenge.  Natural selection’s creative power was, according to Darwin, painfully slow.  It works gradually, slowly accumulating changes in a species over time.  How could one possibly discuss, knowledgably and with experimental evidence, a process that can only be inferred and not seen?

The answer: discuss the fastest form of speciation ever recorded.  This is speciation that occurs in a day.  This is speciation by polyploidy.

Many plants are said to be selfing.  This means that they produce both male and female organs, with the pollen they produce being compatible with their own ova.  They can, and do, fertilize themselves, although they are also capable of reproducing with other individuals.  This strange property of many plants has allowed them to speciate in unusual ways.

Polyploidy is an increase in an entire chromosome set, as we learned earlier on in this series.  If n represents one set of chromosomes, then our sperm and eggs have n chromosomes, our body cells have 2n chromosomes; a polyploid would have anything higher (3n = triploid, 4n = tetraploid, etc).

Imagine that a plant’s meiotic equipment were to break down.  Rather than producing only normal (n) pollen or ova, this plant produces a few diploid (2n) pollen and ova, and then it self-fertilizes.  Occasionally, a 2n pollen may encounter a 2n ovum; the result is an individual with twice as many chromosomes (4n) as its parent.  This is now a tetraploid individual.  This is known as autopolyploidy, because the polyploidy occurs within a single species.  This is in contrast to allopolyploidy, which is polyploidy caused by the breeding of two different species.


Alternatively, and perhaps more commonly, a body cell during mitosis can go through all of the steps of mitosis (DNA replication, separation of sister chromatids) but miss the last step – cell separation.  The cell is suddenly a tetraploid, and it can go on to divide within the organism.  The plant is thus partially a diploid and partially a tetraploid.  The tetraploid segment of the plant, in turn, may propagate more individuals that will also be tetraploid.  Either way, whether ploidy is due to breakdowns during meiosis or mitosis, the result is the same: an instant new species.

What happens when the diploid parent selfs again?  Since 2n gametes are rare, it will likely produce more diploids.  What happens when its freak tetraploid offspring selfs?  It produces more tetraploid individuals, since its ova and pollen, during meiosis, are reduced to 2n, and come back together to form another 4n individual.  Tetraploids, when they appear in the midst of a diploid population, continue to produce more tetraploids.  A new entity has been born.

What happens if one of the diploid individuals is pollinated by a tetraploid?

I’ll need you to review meiosis for you to understand what happens next.  Watch this video, and then we can continue.

The tetraploid plant (4n) produces diploid (2n) pollen.  The diploid plant (2n) produces haploid (n) ova.  When a diploid pollen encounters a haploid ovum, the result is a 3n individual.  So far, so good.  We now have the rise of a third new thing within this population: a triploid.  However, these triploid hybrids often have a difficult problem.  Meiosis involves the pairing up of homologous chromosomes.  In tetraploids, there’s an even number of homologous chromosomes and so everything gets a partner.  In triploids, however, when there is three of everything instead of two or four, some partners get left behind.  The result is inviable gametes.

Triploid plants can produce thousands upon thousands of gametes, but they have such a huge chromosomal unbalance that no offspring can develop.  However, sometimes, albeit rarely, the occasional triploid can produce a fertile offspring.  How?  By restoring the chromosome balance.  This is often achieved by another mistake during meiosis which results in a doubling of the chromosomes within the gamete.  Thus a 3n cell turns into a 3n gamete.  If it were to encounter another 3n gamete, the result would be a perfectly balanced hexaploid (6n) individual.  These, like tetraploids, are usually quite fertile. 

Now, what is a species?  For Dobzhansky, species are separated by a relative inability to reproduce with one another (they might successfully produce hybrid offspring, but if those offspring are sterile, the result is the same as if they had never had children.  Think of a mule, which is the sterile offspring of a horse and a donkey).   In our example of polyploidy, we have diploid plants and tetraploid plants, but any breeding between them is generally disadvantageous, as their offspring are largely infertile.  In a single generation, we went from one happily-breeding diploid species, to two quite distinct species of plants.

What happens if genes cannot pass from one population to another?  Mutations that accumulate in one population will not make it over to the other, and vice versa.  The tetraploids and diploids, although they might live in the same region and be subject to the same selection pressures, will begin to diverge in appearance and life history due solely to the accumulation of different mutations.

Sometimes you don’t even need mutations to bring about differences in phenotype.  The gigas complex is a well-known phenomenon in polyploid plants, in which the polyploids produce thicker stems, grow taller, have larger, thicker, and broader leaves, produce a darker green pigment, and have larger flowers and seeds, than their parental species.  Dobzhansky believed (I don't know if he was correct or not) that this immediate phenotypic change was a direct result of stuffing twice as much genetic information into a little cell.  Polyploid cells tended to be larger than diploid cells, and the structural consequences of this were exhibited in the gigas complex.

Polyploid strawberries produce larger fruit than normal diploid strawberries

Furthermore, many polyploids were able to exist in habitats that their parental diploids could not colonize.  So, ecologically, morphologically, genetically and reproductively, these polyploids were different from their parents. 

Instant speciation.

Differences in the polyploids were even more evident in the case of allopolyploidy.  Elsewhere I have discussed the creation of the species Raphanobrassica by the crossing of a cabbage with a raddish.  The resulting polyploids had the head of a raddish and the roots of a cabbage – not exactly what the breeders were hoping for, since this makes a completely inedible plant – but it was a new species nonetheless.

Production of a new species through allopolyploidy
The species Nicotiana digluta was also formed in the laboratory by crossing N. tabacum (2n = 48 chromosomes) with N. glutinosa (2n = 24 chromosomes).  The hybrids were largely infertile, having 36 chromosomes (24 from N. tabacum, 12 from N. glutinosa) that suffered major meiotic problems due to a serious lack of homologous partners.  But, one of the hybrids was a real rarity.  There was a failure during mitosis in its body cells early in its development, producing a plant with twice as many chromosomes as its brothers and sisters (that is, 72 chromosomes).  Since each chromosome had a partner during meiosis, this plant was quite fertile and was designated as a new species.

The best evidence of speciation by polyploidy comes from simply counting the number of chromosomes that different closely related species have.  There are numerous cases of related but distinct species having chromosomes that are multiples of each other: wheat (related species with 14, 28 and 42 chromosomes, with the original haploid number being 7), Chrysanthemum (18, 36, 54, 72 and 90, haploid number 9) and Solanum (24, 36, 48, 60, 72, 96, + 108 and + 144, haploid number 12), just to give a few examples.

A triploid, sterile trout

By 1932, there were 37 new species of allopolyploids created solely in the lab.  Today, that number is much higher, as the sterility of triploids is being used in interesting ways by different companies.  For example suppose, as has happened in PEI, that you want your trout farm to produce large fish.  There is one problem: trout metabolism shuts down during the winter, and growth slows to a crawl.  But there are other fish with particular genes that allow winter growth, so by adding these genes to your trout, you get transgenic fish that can grow all year long.  This is great for your pocket book.  But what happens if (inevitably) the trout escape, and start breeding with native trout?  You are suddenly responsible for introducing a new gene into the wild, which, generally speaking, is bad for your pocket book.  The solution is to develop a triploid trout.  Since triploids have all sorts of meiotic problems, they will be almost perfectly sterile; you can keep producing your transgenic trout without having a PR nightmare on your hands if the fish escape.

Or imagine there is a pesky mosquito problem.  If you develop triploid males and release them, they will waste the eggs of females, reducing the mosquito population.

Although these scenarios are in fact taken from reality, we need to be really cautious here.  Polyploidy is not just something for the lab.  It occurs in nature all of the time, despite the sterility problems of triploids.  There is simply no guarantee that a transgenic triploid will be 100% sterile. 

Polyploidy has almost certainly played an important role in the evolution of life.  Says Dobzhansky, ‘The prevalence of the polyploid series of chromosome numbers in plants and their relative scarcity among animals constitutes the greatest known difference between the evolutionary patterns in the two kingdoms.’  What this means is that, those who study the evolution of plants must take into account different evolutionary mechanisms than those who study the evolution of animals.  Why is polyploidy so much more common in plants?  It is likely due to the large number of hermaphroditic species of plants (itself likely driven by their inability to move to find mates), and the nature of sex chromosomes in animals.  Having more than two sex chromosomes produces all sorts of developmental problems, including sterility.  However, in animals like fruit flies, where sex is driven by the ratio of sex chromosomes to body chromosomes, and not by the presence of sex chromosomes per se, polyploidy can occur.  Polyploidy is also known in salmonids, certain species of butterfly, oysters, brine shrimp and others.

The evolutionary consequences of polyploidy can be summarized as follows:

1. It is a driver of plant, but rarely animal, diversity
2. It causes rapid (immediate) speciation
3. The gigas complex is a new phenotype that may alter the selection pressures on the plant
4. Having multiple copies of a chromosome does two things:

a) Hides the effects of negative mutations (since if one chromosome receives a mutation, there are still three other functional copies of it)

b) Frees a chromosome to evolve in new directions (if a gene is essential, with mutants being aggressively removed by selection, an extra copy is free to evolve in new directions).  As the chromosomes diverge, eventually the polyploid will become a new diploid

5. It is a rapid means of combining the genes of two different species to produce something novel (allopolyploids only – such as the radish-headed cabbage-rooted Raphanobrassica).   This new, suddenly-produced hybrid has a collection of traits never before seen in nature; the pairing of, say, salt tolerance from the mom with heat resistance from the dad may allow it to colonize areas devoid of either parental species.

6. Polyploid individuals can, themselves, foster new polyploids (a tetraploid could, for example, produce an octaploid).  Chromosome numbers can therefore increase as new species are formed.

For Dobzhansky, polyploids were a vital link in his argument for speciation.  Here was an instance in which reproductive isolation, the defining characteristic of speciation, had evolved rapidly, and its genetic causal basis was known.  Inferentially, then, perhaps the fact that any two species cannot reproduce with each other is also a consequence, not of special creation, but of genetic changes that have occurred as these species have evolved in different directions.  Reproductive isolation in non-polyploids is the topic of the next chapter.

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