Friday, November 24, 2006

Island Mice May Evolve Faster: From One Species To Six In 500 Years



SOURCE: Genome News Network

AUTHOR: Bijal P. Trivedi

COMMENTARY: Allen MacNeill

An alert Evolution List reader has already pointed me to an article that first appeared on April 28, 2000, concerning the unusually rapid speciation of common European mice on the island of Madeira. Apparently, these mice were brought to the island on sailing ships, most likely from Portugal. Since such ships were very small, the total size of the founding populations would have been extremely small; probably less than a dozen individuals (and certainly less than a hundred).

This would certainly qualify as precisely the kind of founder population that I described in the previous post concerning a possible mechanism for chromosomal speciation. In particular, it is extremely interesting that the mice in question have apparently speciated in less than 500 years, and that the mechanism underlying this speciation has involved multiple chromosomal fusions.

Here’s the full article describing the research (commentary follows):

Janice Britton-Davidian spent several weeks in 1999 placing hundreds of mousetraps all over the semi-tropical island of Madeira and discovered what may be an example of "rapid evolution." She caught hundreds of small brown mice that look pretty much alike but that are genetically distinct—a very unusual thing for such a small, geographically contained place. It normally takes thousands to millions of years for one species of animal to diverge to become two. On Madeira, one species may have evolved into six in the space of just 500 years.

Britton-Davidian, an evolutionary biologist at Université Montpellier II in Montpellier, France, showed that populations of Maderian mice have between 22 and 30 chromosomes, even though their ancestors, who first arrived with the Portuguese in the 15th century, had 40.

Madeira is a rugged volcanic island with sharp black cliffs that block all but a few isolated rocky shores. Only a few small villages decorate the strip of coast. The Portuguese were first to inhabit the island, bringing with them the mice that Britton-Davidian so avidly seeks. As the Portuguese founded small settlements around the island, they inadvertently deposited small groups of mice at each stop. And, for the last five centuries, mountainous barriers have prevented these coastal colonies of rodents from commingling.

Britton-Davidian collected hundreds of mice from about 40 locations around the island and found six distinct populations. The common brown house mouse of Europe, presumably the ancestor of the Madeira mice, has 40 chromosomes, but the six families of Madeiran mice have between 22 and 30.

The current families of Madeiran mice are not short of genetic material. They have not lost any DNA. What happened is this: over time, some of the chromosomes fused together, packing more DNA into some chromosomes. Each of the six unique populations of mice on Madeira has its own special assembly of fused chromosomes. Each group of mice may now be its own species.

The diversity of fused chromosomes seems to have occurred in just 500 years, or between 1,500-2,000 generations of mice, says Britton-Davidian. Furthermore, the huge diversity in chromosomes has evolved solely from geographic isolation rather than adaptations to different environments.

"What is surprising is how fast this has taken place," says Scott Edwards, an evolutionary biologist from the University of Washington, in Seattle. Based on fossil records of sea urchins and invertebrates, evolution of different species is thought to take thousands to millions of years. "But this is an interesting case because it may prove to be an extreme case of rapid speciation," says Edwards.

Britton-Davidian wants to know whether these populations of mice have evolved into different species or whether they are on the cusp of speciation. A species is defined as a group of organisms that can mate and produce fertile offspring.

One of Britton-Davidian's most surprising findings is that she and her colleagues found no mice that are hybrids among any of the six groups. "This might be because the hybrids are infertile or they may be less fit than the parents and unable to survive," says Britton-Davidian. Other explanations could be that the groups have been geographically isolated and have not had the chance to mate, or that the mice "recognize each other as different and choose not to mate."

Britton-Davidian has taken some mice from Madeira back to her lab in France and will try interbreeding the six populations to confirm whether the hybrid mice are infertile, which, if they are, would imply that the different groups were in the process of speciation. Her team will also observe the mice to see whether they show behavioral or physical differences.

REFERENCES CITED:

Britton-Davidian, J. et al. Rapid chromosomal evolution in island mice. Nature 403, 158 (January 13, 2000).

COMMENTARY:

I must admit that I did not expect to find evidence supporting my hypothesis so quickly; thanks to list reader Zachriel for finding the article posted above. Several items in the article immediately struck me:

• The mice in question were “seeded” in six isolated communities, presumably unintentionally (i.e. in boxes, foodstuffs, or by climbing down mooring lines). These would qualify as six separate, very small founder populations.

• The mountains separating the six populations would effectively isolate the populations, preventing gene flow and maintaining the populations at very low sizes (i.e. the surrounding environments would not be conducive to allowing the mice populations to expand, as they are adapted to living in human habitations).

• The six populations differ almost entirely in chromosome number, but not in apparent phenotype, as predicted by my hypothesis.

I haven’t had time to follow up and check to see if Britton-Davidian has been able to correlate the chromosomal differences between the six different mice populations and their behavior, etc. As readers of the previous post might suspect, my hypothesis does not necessarily predict that there will be any such differences at all. On the contrary, chromolocal mutations (such as the multiple fusions found in the Madeiran mice) don’t change the genetic information, they simply rearrange where it is located in the genome.

If the foregoing does indeed support my hypothesis (and if the hypothesis eventually is shown to be valid) it says something very interesting about speciation and its relationship to natural selection (and, by extension, the “modern evolutionary synthesis”). According to the “modern synthesis,” speciation is the result of geographic isolation and diversifying selection (as originally proposed by Mayr and Dobzhansky), with selection playing an important role in reinforcing species differences via the intensification of “isolating mechanisms.”

However, my “first-degree inbreeding” hypothesis implies just the opposite: that the genetic processes that isolate populations (which subsequently become species) happen first (i.e. chromolocal mutations, etc.), thereby effectively isolating the populations entirely by accident, and that later the already isolated populations begin to diverge in character as the result of selection, drift, etc.

It also implies very strongly that macroevolution (defined as evolution at the species level and above) actually happens virtually instantaneously, as the result of genomic rearrangements such as chromolocal mutations, with phenotypic diversification taking much longer. This squares with the fundamental difference between cladogenesis (i.e. macroevolution) and anagenesis (i.e. microevolution), as the former is essentially instantaneous at the moment of divergence of a new clade, whereas the latter takes time...lots of time, as Darwin first pointed out.

In closing, it is interesting to contemplate the mounting evidence for surprisingly rapid cladogenesis in nature, as shown by the cichlids of Lake Victoria and the mice of Madeira. As I have said before, these newly emerging ideas are diffficult to reconcile with some of the main tenets of the "modern evolutionary synthesis" (although they fit well with Darwinian theory overall). Once again, "The modern synthesis is dead; long live the evolving synthesis!"

I would really appreciate comments, suggestions, and especially criticisms of the foregoing and of my proposed hypothesis. Just click on my name, below, and send me an email, or just click on the “Comments” link. I’ll get your message either way, and will respond as quickly as ever I am able.

--Allen

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6 Comments:

At 11/25/2006 11:59:00 PM, Blogger Martin said...

Hi Allen,
as I pointed out in the related UD thread your hypothesis can be tested in vivo by the use of MICER clones.
MICER is a method developed by Allan Bradley. It consists of four sets of genomic clones that contain a loxP site in either orientation site and either the proximal or the distal half of a HPRT mini gene. After Cre mediated recombination between the loxP sites of two different MICER clones a complete HPRT mini gene is reconstituted and one can select for the Cre induced alteration of the genome. If the two loxP sites are located within the same chromosome and have the same orientation one will end up with a deletion of the sequences located between the loxP sites. If the loxP sites are inversely orientated Cre mediated recombination will induce an inversion of the sequences between the two loxP sites (it should be noticed though, that without selection prolonged presence of Cre can lead to a reversion of the fragment). If the loxP sites are situated on different chromosomes Cre mediated recombination will lead to reciprocal translocation between the two chromosomes, which is indeed the situation you want to analyze.

MICER clones can be inserted in the respective locus of the genome of murine ES cells via homologous recombination. Thus, it is possible to choose the loci that shall be analysed beforehand. Indeed, one can search for available MICER clones in ENSEMBL (http://www.ensembl.org). If no such clone is available for the locus of interest respective constructs can be easily generated by conventional cloning techniques.

After homologous recombination of two MICER clones in WS cells the translocation can be induced by transiently expressing Cre within these cells followed by selection for the presence of HPRT (for those who are interested: one has to use HPRT negative ES cells for the transfection with MICER clones). Recombined ES cells are subsequently used to generate the respective mouse mutants by blastocyst injection.

In principle one could alternatively breed two different mouse lines derived for conditional gene targeting, which after Cre mediated deletion contain a unique loxP site per haploid genome. One then had to introduce a Cre transgene that is active in the germ line Unfortunately, I don’t know the frequency of Cre mediated recombination in such cases. Thus, I would stay with the MICER approach, because this offers the possibility to select for the desired translocation.
If the translocation is not lethal it can be kept in the offspring by breeding with wild type animals. Homozygousity can later be achieved by sibling intercrosses. If such mice are fertile in intercrossing amongst themselves they can be used to test if they lost the ability to reproduce with wild type mice.

The remaining question is which translocation(s) should be analyzed. Good starting points might be the loci involved in the translocations of Madeira mice. Alternatively, one may look up a comparative synteny map of mice and rats.

Unfortunately, this mouse business is quite expensive: The price per mouse line with a single targeted mutation is about 30000 $. In addition, later you have to face running costs for mouse housing. My guess is that you should not start something like that without a funding of a teast 200000 $ (personal not included).

 
At 11/26/2006 12:26:00 AM, Blogger Martin said...

Many of the commenters at UD have problems to understand with the possible outcome of meiosis in individuals carrying translocations in the germ line. However, there is quite some literature on the inheribility of such mutations in humans (e.g. Angelman-Syndrome and Beckwith-Wiedemann Syndrome). Those who are interested may also look up uniparental disomy that contributes to quite a proportion of these syndromes and may have played a role in the fixation of the genome alterations observed in Maderian mice (for review see: Kotzot D. (2001): Complex and segmental uniparental disomy (UPD): review and lessons from rare chromosomal complements. J Med Genet 38(8):497-507 (free full text)

 
At 11/30/2006 07:39:00 AM, Anonymous Anonymous said...

Amusing article: 500 years and they are still mice. Where is the speedometer? And, what part of those mice are no longer mice?

 
At 2/14/2007 01:53:00 PM, Anonymous Anonymous said...

Could you please explain what you mean by the term "modern synthesis"? Does "Random Mutation + Natural Selection" (RM + NS) capture the essence of meaning of the term "modern synthesis" in your opinion?

 
At 2/19/2007 10:28:00 AM, Blogger Allen MacNeill said...

Two replies:

On the comment "500 years and the mice are still mice" was clearly posted by a creationist. The term "mice" refers to a much higher taxonomic level than species. Therefore, for evolution to have produced a new higher taxonomic level would of course take much more time than to produce new species.

On the other comment/question, no I definitely do not equate the term "modern synthesis" with the creationist strawman "RM + NS." The "modern synthesis" was a synthetic theory founded on mathematical population genetics and supported by mendelian genetics (especially of fruit flies), paleontology, biogeography, and animal and plant anatomy and physiology. It re-established natural and sexual selection as two of the primary "engines" of evolution – specifically, of adaptations – but also identified random genetic drift and other non-adaptive mechanisms (such as the founder effect) as also central to evolution, and especially to phylogenetic differentiation. Since irs heyday in the late 1950s, the "modern synthesis" has been greatly augmented by new theories in population genetics (including kin selection, reciprocal altruism, and group selection theory) and evolutionary developmental biology (also called "evo-devo"), and so many of its central tenets have either been altered or replaced on the basis of new observations.

Equating it to "random mutations and natural selection" is a debating tactic used by ID supporters and other creationists, hoping that participants and observers will accept that equation, which is easily defeated. However, the genuine definition of the "modern synthesis", including all of the modifications that have been added to it since the 1960s is so thoroughly supported by the empirical evidence that no creationist can begin to undermine it, especially since they have no eimpirical data to support their theories.

 
At 2/25/2007 07:26:00 AM, Anonymous Anonymous said...

Two items:

1) I realize that there are other mechanisms involved in the "modern synthesis" but it seems that the most fundamental are RM and NS. As Ayala said, "mutation is the ultimate source of all genetic variation." (Ayala, Francisco J., “The Mechanisms of Evolution,” Scientific American, vol. 239 (September 1978), p. 63). Sexual selection seems to be nothing more than a subset of natural selection. After all, is not sexual behavior natural? As for drift and founder effect, these do not seem to be as fundamental as RM and NS. I think the creationists have a basis for focusing on these two fundamental items.

2) You said the "modern synthesis" is dead, but now you use the same term to include modern speculations about how evolution might work. Shouldn't you use a less confusing term? I like your "evolving synthesis" term you used over at UD.

You think the "modern synthesis" is now dead.

I think the "evolving synthesis" was DOA.

 

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