Is genetics still metaphysical? Part V1/2. A relevant holiday exercise?

It's the holiday season, and what with family and friends, and over-eating (and drinking), one can't operate at full speed.  So I thought that by writing a quick half-post in this series (post V 1/2), I could stall for a day or two before wrapping it up.

Yesterday, as in the past on Christmastime, I took some familiar verse and turned it into some science-relevant doggerel.  In prior years I've mainly reworked well known carols or Christmas songs.  This year I chose some verses that most readers of MT will have been familiar with or even have read in school.  I do it for the fun and challenge, but what exactly does the process involve?  On thinking about that, in the context of the current series of posts about genetic and evolutionary theory, and advances in scientific theory generally, it struck me that the process of writing this kind of doggerel has some inadvertent lessons to teach.

I don't know how you or anyone else cobbles a bit of doggerel together (here, I guess I can't resonate with those of you who take a common view, and think doggerel is so inane that it should be against the law).

I take a well-known poem or stanza, that has long been in my head and that I think most readers will recognize.  This is a form, or we could even think of it as a 'species', with a kind of unity.  My objective is to try to modify that unity to give some other sort of message, but without changing the recognizability of the original.

I try my best to keep as many of the original words as possible, as well as the meter and even the punctuation.  But I substitute words to achieve a very different meaning.  In my obviously amateurish way, I at least try with these new words to keep the phrasing, stress, consonants and vowels as similar as I can.  In that sense, it should 'feel' like the same verse, but have a totally different, unrelated or even reversed message.  Here is how I modified the first 4 lines of Trees:

Original :                                                       My doggerelic changes:                    
I think that I shall never see                          I think that I shall never see
A poem lovely as a tree.                               A gene as lovely as a tree
A tree whose hungry mouth is prest             A gene whose  histones' mouth is pres'd
Against the earth's sweet flowing breast;      'Gainst coiled enhancer's flowing twist;

Reading the new version should feel, in a metric sense and beyond, like the original.  The changes can be humorous, satirical, or poignant, but the new poem should be a kind of new species in the same genus as the original.  It is in that sense an evolutionary product: it did not start from scratch, and it retained the 'fitness' characteristics--the basic framework and substance--of the original.

You can see that no single word-change, not even a groan-worthy pun, can achieve this.  Each new word or modification, alters the meaning of a phrase, or its impact or 'feeling', but in itself would make no sense.  This is obvious, when you look at the famous two lines:

Poems are made by fools like me,                   Genes are named by fools like me,
But only God can make a tree.                         But lonely genes can't make a tree.

Here, my hopefully obvious contrast was of individual causal elements (individual genes) and the composite action of many genes working together.

In a second example from yesterday's post, here is what I did with Browning's very famous sonnet:

Browning:
How do I love thee?  Let me count the ways.
I love thee to the depth and breadth and height
My soul can reach, when feeling out of sight

My doggerelic changes:
How do I leaf thee?  Let me count the ways.
I leaf thee to the depth and breadth and height
My bows can reach, when flow'ring out of sight

For survival as a unit, multiple changes must be made, and there may be many ways to do it (or to try it, at least, as I can tell you from the effort  to make yesterday's doggerel versions worth posting!).   The revision should read, or sound, or feel like the original, even if the overall meaning is profoundly changed.  One can build a new sense to a slight extent, with a single change, but the thing really wouldn't fly until many changes are made and a key point is that the changes must work in trans: they must relate to each other!  As in the original, the various parts interact to generate the end result. Even to be viable as a working intermediate, I find that I must make at least a few changes, but I can vary these, adding or removing some, always going back to the original, as I work towards what (when it's done) I find acceptable.  In fact, if I look back, I can see better ways I might have done it.

This is an evolution, but it is of course not like biological evolution in one very important--and relevant--sense:  I have some goal in mind.  My goal is usually generic, and it may change, so it's not entirely teleological (it leads to 'spandrels', if you're familiar with that famous view of the evolution of novelty), but when I make even my first change test, I have a thought about the general direction.

However, this process does involve a kind of overall, integrative synthesis--the topic of our 'metaphysical gene' series here.  At some point, for an amateur like me at least, it just feels right as a unit.  Each individual change may then be examined and re-modified, but only in the context of the new whole.  For me, it feels as if I have seen the many parts of both the original and the bits I've changed, or other bits I might change, or alternatives in the context of the overall product, just as the original poet had an original, whole in mind.  That is, there is a kind of gestalt change of the whole, not its separated parts, each of which have their own strong and weak points, otherwise unrelated to that overall gestalt.

In my next post, I'll try to  provide some genetically specific examples of the sorts of facts we have in our science, that we know are true, but that we may not be integrating into the kind of gestalt that I've been discussing here.  Perhaps, in a way similar to other changes in science, concentrating on these separate, not obviously similar, facts may help stimulate a whole new picture.

But as I've said already in this 'Metaphysical' series, perhaps the fragmented nature of what we see is, as they say, what there is: perhaps thinking we'll have, or even that we need, a new Darwinian insight, is romantic thinking.  Perhaps life is just a causally messy phenomenon, not one we can unite with a grand synthesis.  Perhaps causal prediction won't turn out to be precise in our field as it is (or at least seems to an outsider to be) in physics.  Maybe life is already the doggerel we've been dealt!

Meanwhile, try it yourself!
If you look again at my tinkered verses in yesterday's post, or even try do do the same yourself with some favorite verse (or take one of my choices and change it in a very different way), perhaps you can get a sense of what I'm trying to convey about the nature of synthesis, how changes are brought about when it must be done in the whole, and with many equivalents, and so on.

Just pick some verse and in a word processor copy it so you can see both versions at the same time. Then with some objective, start modifying, one word or phrase at the time.  Try to keep the meter, basic sounds and stresses, and even the flow of the logic similar, but give it a whole different meaning. In my experience, it's a good kind of enjoyable brain exercise, if nothing else.  It forces you to try to see a whole 'above' its parts, a synthesis one might say, and then make it a different but still functioning kind of 'whole'.

In any case, in my next post I'll try to be clearer about the sorts of facts (the current version of the verse, so to speak) that we face in genetics today.

Redpolls: genetically similar, phenotypically different

Redpolls are a group of small birds in the finch family, members of the genus Acanthis.  They breed in the far north, but sometimes migrate as far south as the central US in winter, when food is scarce further north.  They rely on a small variety of seeds, and sometimes travel a remarkable thousands of miles to find them.

Range of the Common Redpoll; Source: Cornell Lab of Ornithology

All redpolls share characteristic red markings on their heads, but otherwise these birds vary enough that they've been thought to comprise as many as six separate species, based on plumage and morphology.  Most commonly, ornithologists have treated them as three species; the Common Redpoll, the Hoary (or Arctic), and the Lesser.  Now a new paper ("Differentially expressed genes match bill morphology and plumage despite largely undifferentiated genomes in a Holarctic songbird," Mason and Taylor) reports a DNA sequencing study that suggests that the redpolls are in fact a single species.

Common Redpoll; Wikipedia Commons

Arctic Redpoll; Wikipedia Commons; (13667519855)" by Ron Knight from Seaford, East Sussex, United Kingdom -  Licensed under CC BY 2.0 via Wikimedia Commons

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Lesser Redpoll by Lawrie Phipps derivative work: MPF (talk) - Carduelis_cabaret.jpg. Licensed under CC BY 2.0 via Wikimedia Commons

A figure from the Mason and Taylor paper makes the differences more apparent:

From Figure 1, Mason and Taylor, 2015

As Gustave Axelson recently wrote in his post about this study for the Cornell Lab of Ornithology All About Birds blog, seeing a Hoary redpoll can be one of those Moby Dick-like quests for a birder intent on adding it to his or her lifelist.  But Mason and Taylor report, after sampling 77 redpolls of very different phenotype, and sequencing 20,000 SNPs in the genome, and 215,000 in the transcriptome (that is, mRNA transcribed from different genes), with gene expression data and ecological niche modeling, they find very little variation between the different redpolls. In contrast, as Axelson points out, genetic comparisons between other similar species of birds, such as black-capped and Carolina chickadees, has found substantial variation all across the genome.

Mason and Taylor write, "we present evidence of (i) largely undifferentiated genomes among currently recognized species; (ii) substantial niche overlap across the North American Acanthis range; and (iii) a strong relationship between polygenic patterns of gene expression and continuous phenotypic variation within a sample of redpolls from North America."

As evolutionary biologists, Mason and Taylor are interested in the processes that lead to phenotypic diversity and speciation. "The Holarctic redpoll finches (Genus: Acanthis) provide an intriguing example of a recent, phenotypically diverse lineage; traditional sequencing and genotyping methods have failed to detect any genetic differences between currently recognized species, despite marked variation in plumage and morphology within the genus."

Mason and Taylor write that interspecific breeding has been observed, as have birds with characteristics of two different species, though phenotypic variation has been observed to be continuous throughout the redpoll range.  But no one has been able to document significant variation in either nuclear or mitochrondrial DNA.  So, if they are genetically so similar, how is it that these birds look different enough to be considered separate species?  The authors propose three possible scenarios:

The paucity of genetic differentiation within the redpoll complex, despite marked phenotypic variation across a Holarctic distribution, could be the result of multiple evolutionary scenarios (Marthinsen et al. 2008): redpolls may be comprised of (i) a single, undifferentiated gene pool that exhibits phenotypic polymorphism, in which phenotypic differences reflect locally adapted demes or neutral phenotypic variation within a single metapopulation; (ii) multiple gene pools that have recently diverged, in which incomplete lineage sorting has hindered the capacity of previous studies to differentiate populations or species; or (iii) multiple divergent gene pools that are actively exchanging genes through hybridization and introgression via secondary contact.

They compared the niches of hoary and common redpolls and determined that hoary redpolls prefer higher latitudes while common redpolls show less of a preference and are more widespread, with much overlap.  But they don't believe that the difference was enough to explain morphological differences between the birds.  That is, geographic isolation, the usual explanation for speciation, doesn't explain the phenotypic variation observed among redpolls.

Mason and Taylor note that the lack of outlier SNPs suggests that the different redpoll species, as now recognized, share a very recent ancestry.  If there were outliers, this would suggest that the birds had had a long history of no contact, during which time genetic variants arose and spread, but then the species reunited, and the interbreeding would have dispersed much, but not all, of those variants between the entire family.  That is, option i above; this is a single undifferentiated gene pool that exhibits phenotypic polymorphism.

Intriguingly, we found novel differences in gene expression that are correlated with redpoll phenotypes, suggesting that gene expression might play an important role in generating phenotypic diversity among redpolls.

This is intriguing.  Mason and Taylor suggest that redpolls should now be considered a single species,  although as Axelson says, this is up to the American Ornithologists Union.  But, given the very low genetic diversity even between widely dispersed birds, and the fact that phenotypic variation is continuous within the genus, it makes sense.  They further suggest that gene expression differences could be due to environmental conditions which trigger phenotypic plasticity in traits like bill width or plumage coloration.

Without whole genome sequencing, these results remain suggestive.  There may be as of yet unknown regions of the genome that are responsible for the variation seen in this species, but the lack of variation in SNPs throughout the genome suggest this is probably not going so.

Evolutionary considerations and the species problem
Evolutionary biologists know that there is a 'species problem'.  That is, only individuals are clear-cut distinct natural units (and, given their colonization by bacteria and the like, even they aren't all that discrete).  Species would be next, but it is about group properties and there are many definitions.  The most commonly accepted is that a species is a group of individuals that can successfully mate and produce fertile offspring.  Similar individuals whose offspring are always sterile would be assigned different species.  Different appearance need not imply mating incompatibility (as, for example, people from Africa and Polynesia, who are inter-fertile).

Single genetic changes have been found to lead to mating incompatibility, as between populations of fruit flies.  Of course changes of any sort can do this in the case of individual human couples.  If there is mating incompatibility among groups, at least, we call them different species.  Among other reasons, the expectation is that over time they will diverge in their genes and traits, with or without the aid of natural selection, and become ever more different.  Only with shared mating would these differences be blended and circulated through a species' population.

We can note four important points here.  First, species can be defined in many ways, but the idea of genetic isolation as an enabler of separate adaptation and divergence, that goes back to Darwin, is important in accounting for the evolution of diversity.  Second, speciation is a separate phenomenon from diversity of traits.  The latter is found both within and between populations of the same species. These are obvious but subtle points, often missed or overlooked even by biologists who equate natural selection and trait differences with species differences.  Mating incompatibility enables the accumulation of trait differences, but trait differences do not in themselves enable speciation.

Thirdly, what we haven't mentioned yet, is polyphenism.  This is a well-known phenomenon in which the same genotype can yield very different phenotypes (traits) in different environments.  This can happen if something in the diet produces pigments, or it can happen if genes are expressed, or not, depending on environmental conditions, leading to environment-specific results, in different individuals with the same genotype or the same genotype in different environments.  For example, the brown goldfinches in our back yard are turning yellow as spring comes.

Fourth, individual groups whose members could physically and genetically mate successfully, but don't, either because they are isolated from each other, don't come into contact, or just simply don't do it even if they could, are sometimes considered to be different species.  Usage varies and it's a judgment call, with  no external 'law' necessitating the definition.

There is no one principle or rule about by which biological species can be defined by trait comparisons, or genomic comparisons alone.  Each case is different, and since genotypic differences  or trait differences can, but needn't indicate, species differences, one has to study each case on its own merits.  That's not always easy, but it's the nature of life.

Variation in levels of gene expression are easy to document but hard to interpret

Has gene regulation been a significant player in speciation and adaptive evolution?  It has long been assumed that the answer to this is yes, and the prevailing view is, in essence, that everything that we see must have been screened by natural selection, except for such things as minor variation or measurement error, including the regulation of gene expression.

However, this is as much a faith as a fact, and a paper in the July Nature Reviews ("Comparative studies of gene expression and the evolution of gene regulation," Gallego Romero et al.) systematically reviews the evidence based on new molecular techniques, and suggests that it's a hard question to answer.

The assumption, based on comparative studies, is that much of the variation in gene expression is due to genetic variation and is heritable. 

This finding provided a strong motivation for comparative studies to focus on expression levels as an important intermediate molecular phenotype: one that ultimately determines heritable variation in complex morphological and physiological phenotypes, including traits that evolved under natural selection.

Gallego Romero et al. describe the state-of-the-art technologies that have been used in this work, including RNA sequencing (RNA-seq), which has replaced microarray analysis in many instances.  RNA-seq allows more precision in estimating gene expression levels, which is important for this work. RNA-seq sequences every copy of mRNA extracted from a given set of cells of some chosen type. The more times you see the same gene's mRNA, the higher the expression level.  For microarrays, the concentration of a given gene's message was less easily quantifiable.

Assessing the effects of gene regulation on evolution naturally enough encourages evolutionary biologists to try to identify selective scenarios that might explain variation although, as the authors say, "To do so, it is necessary to distinguish between the environmental and genetic effects on gene regulation as well as to control for a large number of potential sources of variation and error" (which can be environmental or experimental). 

To do so, it is also necessary to believe that speciation is always due to natural selection.  Gallego Romero et al. do cite previous discussion of whether gene expression variation is always such, and clearly themselves recognize that the answer is not necessarily straightforward nor uniform.  Gene expression evolution may be due to selection -- often stabilizing selection, which eliminates the extremes, but sometimes directional, meaning that there would be positive benefits to increased expression -- or it may be neutral, that is there's no measurable effect on fitness when expression varies. But, as the paper also says, "Alternative explanations for gene expression differences between species, such as consistent inter-species differences in environments, are often difficult to exclude, especially in primates."

In other words, a definite 'maybe'!

Another complication includes the possibility that gene expression levels may vary by tissue, which at least one comparative study showed.  Indeed, as Gallego Romero et al. suggest, documenting variation in gene expression levels across species is the easy part, whatever tissue you choose to use, so long as it's the same for the different species.  But there are many issues in deciding what to look at.  Making sense of it is much more complex because of questions of how much is due to genetic variation, regulation, environmental influences, explaining underlying molecular mechanisms and so on.

Although progress has been slow, it is now possible to identify functional elements of DNA from nucleotide sequence analysis.  Gallego Romero et al. predict that it will one day be possible to predict gene expression patterns from the sequence of their regulatory elements.  However, all the same caveats will continue to be true -- gene expression is affected by environmental and epigenetic (non-sequence related changes in DNA) variables, and these will continue to be unpredictable.  The authors predict, though, that the use of stem cells will one day make "a reality detailed mechanistic functional studies of gene expression evolution in primates."  Stem cells could be induced to behave like, say, liver or kidney or skin cells.  Whether they will express genes in the same way out of tissue context as in it is another question.

This paper raises the question of what gene expression variation can tell us about phenotypic evolution, and points out that with new molecular techniques we can document gene expression levels in more detail than ever before.  But what these levels actually represent is another question, since, as the paper points out, there are many variables than affect gene expression levels.  And, there are numerous reasons for cross-species changes in gene expression levels, including but not limited to natural selection.  Indeed, one can imagine that speciation may precede changes in gene expression levels. Or that expression levels just change due to chance changes in the mechanism that don't affect the organism or its 'fitness'.

And as with most aspects of life, there are going to be multiple explanations for speciation.  Gene regulation may explain some, but, e.g., Allen Orr is among the more prominent evolutionary biologists documenting genetic causes of speciation such as mutations that create hybrid sterility, or genes that have no harmful effect within a species but when combined with genes from another species cause sterility.

There is no one way and no way to infer from expression differences what their origin might be.

Getting past evolutionary pointilism--or creationism in the journal Nature?

The July 15 issue of Nature, in true Nature style, has a high human-interest picture of a fossil cranium fragment (glaring at you from the cover!) that purportedly shows that the separation between ancestors of Old World monkeys and apes had occurred. The find was in Saudi Arabia, and while Holly is the person most appropriate to discuss the details, we have a few words to say about it until she does.

The fossil is about 29 million years old. It does not have a specific trait found only in modern Old World monkeys, but not in apes. If the interpretation is correct, and we have no reason to question it based on our own fragmentary knowledge of this area, then it does suggest that the monkey-ape divergence occurred subsequent to when this individual lived.

Fine. Our issue, and it's yet another complaint about Nature's drive to be a pop-culture rather than serious scientific journal, is with the heading: " Parting of the Ways: Saudi Arabian fossil pinpoints divergence of Old World monkeys."

The implication in Nature is almost creationist in nature. It is the assumption that this lump of one-time bone was at the 'parting' of the ways, and that such events occur instantaneously. If not, how could a specimen 'pinpoint' the separation?

In fact, speciation is a gradual, statistical, probabilistic population phenomenon. It does not generally occur in a moment.

But suppose this is science, not Creationism on Nature's part. Even then, what is the chance that this particular specimen, or even any specimen from thousands of square kilometers or thousands of generations around this time, was the 'point' of speciation? The odds are minuscule, and in a deeper sense untestable.

Speciation, in the usual definition, would be the time at which no individual from either of the two new-lineage populations could successfully mate. But for thousands of generations, gradual divergence would in reality merely have diminished the probability that a random male from one and female from the other ancestral population could have mated successfully.

Even a mutation that by itself would make such mating impossible would not have spread throughout one of the populations so that the two species lineages were suddenly discrete and immiscible.

To melodramatize speciation and evolution in a way that almost makes it creationistic is yet another editorial decision by the journal that shows either crass grabbing for sales, the superficial understanding of science even by scientists or science journalists, or the simple dumbing down of science. The last thing it is, is a contribution to evolutionary science (we note that this is the editors' fault, not the authors: their paper makes none of these idiotic claims. Instead, they say that the fossil record may now show that the split happened during a 5 million year period after the demise of this current individual).

Darwinism without Darwin: The Origin of Species without Natural Selection?

We've written here before about whether Darwin actually solved the species problem for which he named his famous book. We concluded that he did not--natural selection, geographic distance, adaptive responses to environmental changes, time since common ancestor, none of these necessarily lead to speciation, though together they constitute the processes that explain biological divergence, adaptations to environment, and ultimately mating incompatibility (the most common practical definition of species). The question of what causes speciation at the gene level is currently being addressed by molecular biologists,who have advanced various ideas, and this is what Allen Orr, from the University of Rochester, talked about at the meeting in Italy.

Allen has been publishing on this question for a long time based on evidence found in fruit flies. He crosses two particular lines of flies, one from the US, and one from Colombia, and finds that their offspring are either sterile or a process called segregation distortion or meiotic drive results in an overwhelming proportion of offspring of just one sex (male or female, depending on the particular cross), so that the F1 (offspring) generation can't reproduce. They thus cannot form their own population, which demonstrates that, in this sense, the US and Columbian populations are separate species.

As we understand his work, the effect is not 100%, so by classical concepts the speciation is not complete, but this is a detail rather than a profound aspect of the results, which indicate that genetic mechanisms--or genetic 'conflict'--can be responsible for speciation, rather than the classical Darwinian idea that it is a suite of adaptations to the environment that leads to species formation.

Five or six genes, including several found in Orr's lab, have been shown to be responsible for these processes. They have nothing in common, according to Orr, except that they are evolving very fast. They are not related to particular adaptations to climate, diet, predators, pathogens, and the like. Instead, they can be referred to as 'hybrid sterility' genes, and a number of such genes or mechanisms have been found over the years, indicating that this particular example is not unique.

Hybrid sterility was discussed at some length by Darwin in the Origin of Species, and the phenomenon was well-known in his time, though of course nothing about its genetics. The interesting fact, perhaps, is that mating between such species leads to offspring, which one would think meant the parents were not separate species after all, but the hybrid cannot reproduce. This is quite different from the inability of, say, dogs and cats to mate with each other (should they even want to!). Nobody doubts that, by any definition, dogs and cats are different species.

The interest in hybrids is that they are formed from closely related 'species', such as members of the horse family (or fruit flies, these days), so hybrid sterility seems relevant to our understanding of the process by which species differences arise.

Darwin was wrong in many respects. Indeed, one can find flaws, shallow evidence, forced reasoning, and speculation throughout his work. He was thoroughly wrong about many things, perhaps most notably the nature of inheritance, the inheritance acquired traits, and the age of the earth (and he was quite anthropologically naive in terms of his ideas about the evolution of human 'races', or those with different cultures). Thus, Darwin's work is not a 'revealed' truth the way some people take the Bible or other sacred texts to be.

Instead, Darwin's work is masterfully integrative, assembling grand ideas from a wide diversity of carefully considered data. Given the data of his time, his deep insight was that life is a history of process rather than separate creation. Once that idea dawned on him, he was incredibly capable of developing the case. The proof of that is the same fact: his overall idea withstood the many errors that he made about the details. That is a powerful test of any scientific idea.

Indeed, the 'species problem' (or 'transmutation' as it was often called then) is a rather trivial technical issue, of interest to systematists (those who build trees of biological relationships). The species relationships were key to Darwin, because they showed that life was a history and as he said extensively in the Origin, he could see no better explanation than his (and certainly not creationism) to account for the diversity of facts that he presented.

What problem was Darwin trying to solve....and did he actually solve it?

We properly honor Darwin on the 150th anniversary of his Origin of Species, though more proper would be to have honored both Darwin and Wallace last year, when their ideas were jointly presented to the Linnaean Society. Indeed, their ideas actually rest on the cell theory, which was presented by Virchow in the same year (1858).

At the meeting Ken attended in Brazil last week, he got involved in a discussion with the distinguished ecologist Doug Futuyma of SUNY/Stony Brook. Ken had asserted that despite the title of his book, Darwin had not, in fact, solved the 'species' problem. First, beyond individuals, species are the nearest we have to objective categories in nature. Usually, we define species as populations that cannot interbreed to produce fertile offspring. But even there our definitions are often vague or imprecise.

Variation, even genomewide variation, can exist without speciation (it does among individuals within every species!). Widespread adaptive variation can exist without leading to speciation (humans are variable worldwide for presumably adaptive reasons--e.g., skin color, yet we're one species). And mating barriers can arise without adaptation in the usual sense (e.g., hybrid sterility genes).

In that sense Darwin did not solve the species problem he named his book after. Doug Futuyma suggested, however, that Darwin's main objective was not speciation per se, but the process that leads to it. Indeed, Darwin wanted 'natural selection' in the title of his book, because that was the process he was invoking as an extension of artificial selection by breeders, to explain long-term biological change and the origin of adaptive structures.

But was 'species' an incidental interest or a primary one? We think the answer is that species was indeed a central objective, and yet it is not separable today, nor in Darwin's mind, from the ultimate result of the process which is speciation. This seems clear in the way Darwin's book was written, in the materials presented to the Linnaean Society, and also in letters he wrote around the time of the book and earlier, around 1844, when he drafted a private sketch of his ideas.

The process was an extension of agricultural and hobby breeding, that clearly led to variation. But Darwin was also determined to show that species--natural 'types'--were not the result of specific acts of creation. The nature of 'transmutation' as it was often called at the time, was hotly debated and of course then, as now, centrally involved religious explanations of the world. Darwin was convinced that 'varieties' and 'species' arose gradually through natural processes.

So, while he did not solve the species problem per se (which is not a 'neat' problem in any case), he provided brilliant insight as to the nature of the processes that, in various ways, are involved in natural divergence that leads to the origin of species.

Origin of species?

2009 is being celebrated as the 150th anniversary of Charles Darwin's famous book On the Origin of Species . . . . whose full title continued by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. Actually, 2008 was a more legitimate anniversary to celebrate, because it was a year earlier that Darwin's and Alfred Wallace's papers suggesting that species arose by the action of natural selection were read before the Linnaean Society in London.

We rightly celebrate Darwin's contribution to science, which clearly was among the most incisive, sweeping, and transformative scientific revolution that has ever occurred. The theory of evolution by natural selection has become the clear core of most of the life sciences, and its ideas have been borrowed by social and physical sciences--even by cosmology and astronomy (yes! where universes are seen as competing ecologies of galaxies, coming and going via black holes, based on their basic properties, etc.).

But was the Darwinian theory correct?

Natural selection is certainly a phenomenon of life, and it can lead to changes in traits whose basis is heritable (generally, this means is 'genetic', or encoded in DNA). Darwin equated that with the same process that leads to speciation. Over time, organisms become differentiated by virtue of the adaptive differences that arise by natural selection in different environments, and these adaptive differences make for new species. Clearly this can in principle lead to mating incompatibility, the criterion usually accepted as a definition of species, and once mating no longer occurs the populations, that started out as one, can diverge more and more. Hence, over very long time periods, we have sea creatures diverging into fish, reptiles, and mammals. Indeed, we have plants and animals diverged from single ancestral species.

But the relevant questions these days does not have to do with divergence from common ancestry nor how traits might evolve, nor even the definition of species, but the process of speciation itself. That is still not well answered, and facile Darwinian explanations don't work nearly as well as they are said to. In fact, in many ways they are as vague and assumption-bound -- and perhaps as wrong! -- as they were in Darwin's day, and for the same reason.

When populations are separated for long time periods, genetic differences arise among them. Mutations occur locally in each population, but they are relatively rare and basically unique at the DNA level. That's because the very same mutation, say an A to a G at some specific spot in DNA, only occurs once in every ten to hundred million parent-offspring transmissions, roughly speaking. Populations in each region occupied by a species will accumulate such differences across their entire genomes. These changes will have a range of effects -- some none at all, others affecting the organism's traits. Selection may or may not prefer one version over the other.

The upshot is that regional differences arise. Darwin thought these were mainly due to selection's screening of the variants, leading to different local adaptations in populations of what had been a single species, and hence to mating barriers.

This is true only if the changes affect mating compatibility, because sperm fails to fertilize eggs, or the individuals don't choose to mate, etc. But just having, say, different shaped beaks doesn't mean you can't or won't mate (if you're a bird). In fact, humans occupy the proverbial ends of the earth, and those in Tierra del Fuego have been isolated from those in southern Africa for fifty to a hundred thousand years (or more), they look very different, their genomes are so different that one would never mistake a Fuegian for a San. Yet they are sexually compatible. The same is true of baboon species that have been separated for millions of years. In both these primate examples, the regional genetic differences are genome-wide, not just in a gene here and there. And these are just a couple of many examples.

Yet the opposite can also be true. Ring species are those occupying a long linear region, in which individuals from adjacent parts of the range are mating-compatible, but individuals from the ends of the range are not. Yet, these are considered the same species. Ring species show the subtle nature of speciation (and, by they way, humans have not become a ring species despite long separation).

At the same time, single mutations can make mating incompatible in what are otherwise clearly the same species. Known mutations of this type are called 'hybrid sterility' mutations and several examples have been studied. Single mutations or chromosomal changes can lead to mating incompatibility, and hence effectively set up different species, with no other 'adaptive' changes in the Darwinian sense. Likewise, a substantial fraction of human matings, even within a single population (e.g., infertile marriages) shows that the usual kinds of physical and behavioral traits need not arise by Darwinian processes, in order for new species to form. Unless, of course, one wants to 'save' classical Darwinism as a dogma by defining the responsible mutations as being 'adaptively' different. Nothing we've said here invalidates the ideas of common ancestry and the potential of natural selection to mold traits, and mating-incompatibility mutations may literally be viewed as 'adaptations', but that distorts the meaning of adaptation and natural selection.

These are profound facts. They show that there are still many important problems, central problems, to work on in biology. Despite Darwin's brilliant insights, some of his basic reasoning and objectives were not as correct as they have been viewed for 150 years.

Singing along

We heard a BBC discussion today about urban birds in Britain. An interviewee, a bird expert of some sort (we did not catch his name or profession, but he seemed to be a biologist), was describing the development of locally different dialects in urban areas of the country. The local birds recognize each others' 'language', but these are different among localities. When played the call of a bird of the same species, but with a different 'accent', birds didn't respond with nearly as much interest as when the call was of a bird from the same locale as the listener.

This is interesting, because there is so much stereotyping in popular culture, guidebooks, and the like, that describes what 'the' so-and-so bird does. But over time, for all sorts of animals, domestic and wild, local speech dialects have been detected, so the story here is not a great surprise. The idea here is that in each city, birds become more distinct over time, so that they no longer recognize each other's songs.

The discussion then took a rather predictable evolutionary turn. If these birds continued to have locally differing dialects, then birds from different areas could no longer communicate to mate, and this would lead to the evolution of new species. Partly, this is simply a matter of our own--the scientists'--definition of what a species is. There, there's not really a difference (that one can test) between 'don't mate' and 'can't mate', and in either case we declare the two groups to be different species.

This is classic, but rather superficial Darwinism, one of the issues we write and think a lot about. There is nothing wrong with the logic itself. Long-term isolation is likely eventually to lead to the accumulation of so much genetic difference that members of each area could no longer mate successfully.

But how long does this take? Probably hundreds, or thousands of generations (or more). Think about that in this context. How stable are urban areas in a place like Britain, relative to such long times? For birds, that would mean centuries or millennia (or more). Given the rapid change of urban landscapes, transportation, and environmental changes, the odds that simple local dialects, which have been observed to develop in a short period of time, would persist or remain sufficiently isolated for such lengths of time seem remote, even if certainly not impossible in principle.

Species can remain mating-compatible even after hundreds of thousands or even millions of years of separation. Humans (who have dialects if any species do!) inhabit the entire terrestrial globe, and at the end points (the tips of South America and Africa) have been isolated for around 100,000 years (5,000 generations at least), and are still fully mating-compatible.

Oversimplified evolutionary explanations are pat, often irrefutable because untestable, and the problem is that they cover over some of the more interesting questions about how things actually happen (one of the issues we raise in The Mermaid's Tale). Speciation may be due to the accumulation of large amounts of small genetic differences due to local adaptation (behavioral, such as by mating calls, or otherwise); that was certainly Darwin's idea of what happened. But this need not be so. Small genetic changes in chromosomal compatibility can also lead to mating isolation (some of these are called hybrid sterility mutations), without any of the usual kinds of adaptations due to natural selection. And what happens over eons of time is unlikely in most or at least many cases to be easily extrapolated from what is observed in just a couple of generations.

It's for this reason that we caution against such simplifications. They give a semblance of understanding according to a widely, if often uncritically, accepted theory. But they are a reflection of scientific impatience that can obscure the facts that may be important for a deeper understanding.