The Modern Evolutionary Synthesis

In the years following the publication of the Origin of Species in 1859, Charles Darwin’s theory of evolution became widely accepted throughout most of the scientific community. Other naturalists, including such notable figures as Charles Lyell, Joseph Hooker, Asa Grey, and especially Thomas Henry Huxley quickly came to accept Darwin’s assertion that what he called “descent with modification” had in fact occurred.

However, scientific opinion was much more divided on the subject of natural selection, Darwin’s proposed mechanism for evolution. To understand why, consider the three preconditions Darwin proposed as the necessary prerequisites for natural selection. They are:

• Variation: There must be significant differences between the members of an evolving population. These variations need not be extreme, as illustrated by the relatively large changes that animal and plant breeders have accomplished, using relatively slight differences in physical appearance and behavior.

• Inheritance: The distinct variations noted above must be heritable from parents to offspring.

• Fecundity: Living organisms have a tendency to produce more offspring than can possibly survive. Among those individuals that do survive, those that also reproduce pass on to their offspring whatever characteristics made it possible for them to survive and reproduce.

Given these prerequisites, then the natural outcome is:

• Non-Random, Unequal Survival and Reproduction: Survival and reproduction are almost never random. Individuals survive and successfully reproduce because of their characteristics. It is these demographic characteristics that form the basis for evolutionary adaptations.

Considering these four ideas, we can ask the question, “What is the ultimate source of the new characteristics that are preserved and promulgated from generation to generation?” The answer is, “The ultimate source of all new characteristics is the ‘engines of variation’ – that is, those processes that produce the natural variation between individuals that Darwin emphasized as being absolutely necessary for the operation of natural selection". In a nutshell:

Variation between individuals is the key to evolution by natural selection.

However, in the Origin, Darwin summarized his presentation of his views on variation with this statement:

"Our ignorance of the laws of variation is profound."

Neither Darwin nor any of his contemporaries (that he knew of) had a coherent theory of heredity or variation. However, this was not an insuperable obstacle to Darwin. Instead of giving up his argument, he simply accepted as a given that many important traits of animals and plants are heritable (pointing again to the observable facts of inheritance in domesticated animals and plants). He also proposed that, although he had no explanation of how they arose, variations among the members of a species do indeed occur, and can provide the raw material for natural selection.

There were therefore two reasons why Darwin’s proposed mechanism of natural selection was not widely accepted, even among scientists:

• Many of Darwin's contemporaries (and, in fact, Darwin himself) believed in Lamark's assertion that acquired characteristics could be inherited through use and disuse. This process directly contradicts the blind and purposeless process of natural selection, and therefore held the door open for purpose in evolution.

• The consensus among naturalists was that inheritance worked by "blending" the characteristics of parents, which would cause any incipient adaptations to be diluted out of existence.


This second objection to Darwin's mechanism of natural selection was almost fatal to his theory. In an influential review of the Origin, written in 1867 by Fleeming Jenkin (a very well-respected English engineer and designer of the first trans-Atlantic telegraph cable), Jenkin pointed out that blending inheritance would eliminate variation within a few generations:

“However slow the rate of variation might be, even though it were only one part in a thousand per twenty or two thousand generations, yet if it were constant or erratic we might believe that, in untold time, it would lead to untold distance; but if in every case we find that deviation from an average individual can be rapidly effected at first, and that the rate of deviation steadily diminishes till it reaches an almost imperceptible amount, then we are as much entitled to assume a limit to the possible deviation as we are to the progress of a cannon-ball from a knowledge of the law of diminution in its speed.”

If (as most naturalists of Darwin's time believed) all traits were blended from generation to generation, all of the distinctiveness of each variation would be lost and the population would remain essentially unchanged. Darwin got around this objection by proposing that large numbers of new variations (i.e. mutations) occur with each new generation. He called these “continuous variations,” but did not propose a mechanism for how they might be produced.

Mendelian Genetics


However, at about the same time that Darwin was working out his ideas on natural selection and evolution, Gregor Mendel was working out a revolutionary new theory of genetics. Mendel was born in 1822 in Moravia, a province of the Austrian Empire (now part of the Czech Republic). Because he was a peasant's son, Mendel was expected to return to the family farm after finishing his education. However, Mendel was not satisfied with all that he had learned. The university, instead of answering his questions, instilled in him an insatiable curiosity about nature.

Mendel observed that some offspring of some organisms had traits that were similar to only one parent, rather than being intermediate between both. He explained this phenomenon by assuming that heredity was determined by tiny, discrete “particles of inheritance” that were passed from the parents to the offspring via the reproductive cells. This would explain how some traits could remain unblended in the next generation.

Such thinking stemmed from Mendel's university education in physics. Ever since Isaac Newton revolutionized the science of physics, all of nature has been considered by physicists to be subject to "natural laws" based on the existence of and interactions between small, indestructible particles of matter. The goal of a physicist is to learn about the laws that determine the behavior of the particles, and to use such laws to predict the behavior of material objects subject to natural forces, such as gravity. Central to this intellectual tradition is the idea that an investigator can often work out these laws through careful observation and experimentation.


Mendel believed that these same methods could be used to study inheritance in living things. Having become established as a monk in an Augustinian monastery in the city of Brünn (now Brno, in the Czech Republic). Over a period of seven years he studied the inheritance of various characters in garden peas. In his landmark paper, "Experiments in Plant Hybridization” ("Versuche über Pflanzen-hybriden" in the original German, published in 1866), Mendel tells how he used the garden pea plant to study the laws of heredity.

Mendel's techniques differed from those of other investigators in three ways:

(1) He looked at one trait at a time;

(2) He followed this trait from generation to generation over eight years; and

(3) He used larger numbers of organisms in his studies. At the end of his experiments, he had carefully observed over 29,000 plants.

In his most famous set of experiments, Mendel studied 22 varieties of plants of the same species: the common garden pea (Pisum sativum). He studied a total of seven different traits, each with two alternative forms, including seed shape, color, and seed coat color; pod shape and color, flower position on the stem, and stem height.

For example, in one series of experiments, Mendel crossed pea plants that produced round seeds with pea plants that produced wrinkled seeds, and then observed what kinds of seeds were produced as the result of this cross over two generations.


Mendel observed that the two forms of each of these traits did not blend with each other. Among the offspring of the first cross, only one form of each trait showed up; the alternative form seemed to be lost. For example, when peas with round seeds were crossed with peas with wrinkled seeds, the first generation of offspring only produced round seeds (as shown in the Punnett square, above).


However, in the second generation, the seemingly lost form showed up again. In our previous example, wrinkled seeds showed up again in the second generation of offspring, comprising approximately one-fourth of all of the offspring of that cross. Mendel explained this result by saying that the lost form of each trait was actually latent or cancelled by the expressed form. He called the prevailing form of a trait dominant and the latent form of a trait recessive. Mendel's definitions of dominance and recessiveness are sometimes called Mendel's Law of Dominance:

Dominant traits mask the appearance of recessive traits whenever dominant and recessive traits are combined in one individual.

In our example, the gene for seed shape has two different forms. One form produces round seeds; the other form produces wrinkled seeds. Different gene forms that produce different forms of a trait are called alleles (from the Greek allos for "other"). In this example, the allele that codes for round seeds is dominant to the allele that codes for wrinkled seeds.

Mendel observed that dominant and recessive forms of a trait did not become blended. Instead, the recessive form of the trait reappeared in an unaltered form in the second generation. Based on this observation, Mendel formulated his Law of Segregation, which states that:

The different forms of a trait remain separate and unblended from generation to generation.

Mendel was so convinced of the validity of his conclusions that his subsequent work with other plants, some of which failed to support his hypothesis, did not discourage him. As he wrote in 1866,

"It requires indeed some courage to undertake a labour of such far-reaching extent; this appears, however, to be the only right way by which we can finally reach the solution of a question the importance of which cannot be overestimated in connection with the history of the evolution of organic forms."

Late in his life, Mendel's time was mostly spent fighting political battles for the monastery and peasants of his village. In his lifetime, Mendel witnessed a complete change in his homeland. In his later years, the focus was no longer on agricultural advances but on political advances. The rise of the Hapsburg dynasty and the consolidation of the Austro-Hungarian Empire forced different values on the people. The days of intellectual freedom, when a monk could study agriculture in a monastery garden without interference by the government, were drawing to a close. Shortly before his death in 1884, Mendel said to a future abbot of the monastery:

"Though I have suffered some bitter moments in my life, I must thankfully admit that most of it has been pleasant and good. My scientific work has brought me a great deal of satisfaction, and I am convinced that it will not be long before the whole world acknowledges it."

Evolution by Mutation

Mendel's belief that his work would eventually be recognized was not mistaken. In 1900, only fourteen years after his death, his work was simultaneously rediscovered by three different geneticists – Carl Correns, Erich Tschermak, and Hugo de Vries – working in three different countries. They each realized that Mendel's particulate theory of inheritance fit patterns of inheritance they were observing.

It is interesting to speculate what Darwin would have thought had he known about Mendel's work. Genes that did not blend in each generation were the answer to Darwin's dilemma, and could have put him onto the right track as early as 1866, the year Mendel's most important paper was published. A copy of the journal containing Mendel's paper was found in Darwin's library at Down House, but it had apparently not been opened or read.

There is an even deeper irony: the rediscovery of Mendel's work led geneticists to reject natural selection as the mechanism for evolution, in favor of mutations. Hugo de Vries, one of the rediscoverers of Mendel's work, proposed that mutations (i.e. changes in the phenotype of an organism, occurring in just one generation) were the primary "engine" of evolutionary change. De Vries did his pioneering work in genetics using the evening primrose (Oenothera lamarkiana), which is now known for having sudden, large mutations (called "macromutations") in its overall phenotype.


De Vries argued that these kinds of mutations were the basis for the changes in phenotype to which Darwin referred in the Origin of Species, and that therefore natural selection was neither necessary nor likely as a cause of evolutionary change. Indeed, DeVries asserted that macromutations were responsible for the "origin of species", and that natural selection played little or no role at all in this process. The mutational theory of evolution promoted by DeVries and other pioneering Mendelian geneticists was accepted by most of the prominent geneticists at the turn of the century, and led to widespread public testimonials that "Darwinism was dead":

“Today, at the dawn of the new century, nothing is more certain than that Darwinism has lost its prestige among men of science. It has seen its day and will soon be reckoned a thing of the past. A few decades hence when people will look back upon the history of the doctrine of Descent, they will confess that the years between 1860 and 1880 were in many respects a time of carnival; and the enthusiasm which at that time took possession of the devotees of natural science will appear to them as the excitement attending some mad revel.” - Eberhard Dennert, At the Deathbed of Darwinism (1904)

The Hardy-Weinberg-Castle Genetic Equilibrium Law

However, like Mark Twain, reports of Darwinism's death were "greatly exaggerated." In the second decade of the 20th century, three other researchers, again working separately and mostly unbeknownst to each other, proposed a theory that would eventually lead to the re-establishment of natural selection as the prime mover of evolution.


G. H. Hardy, Wilhelm Weinberg, and William Castle all proposed a mathematical theory that describes in detail the conditions that must be met for evolution to not occur. This theory, often called the Hardy-Weinberg Equilibrium Law lays out the conditions that must be met for there to be no changes in the allele frequency in a population of interbreeding organisms over time.

Recall Mendel's definition of alleles: different forms of the same gene that produce different variations of a trait. In the context of evolution, alleles are what code for the phenotypes that change over time in an evolving population. Therefore, changes in the alleles present in a population will produce changes in the phenotypes present in that population. This, in a nutshell, is the genetic definition of evolution:

Evolution is the result of changes in allele frequency in a population over time.

What Hardy, Weinberg, and Castle all realized is that for allele frequencies to not change in a population, five conditions must be met:

• There must be no mutations (i.e. alleles cannot change into other, different alleles).

• There must be no gene flow (i.e. individuals cannot enter or leave the population).

• The population must be very large (i.e. random accidents cannot significantly alter allele frequences).

• Survival must be random (i.e. there can be no natural selection).

• Reproduction must also be random (i.e. there can be no sexual selection).

Notice that the Hardy-Weinberg Equilibrium Law seems to say only that there are conditions under which evolution can't happen. Aren't we interested in those conditions in which evolution can happen? Yes, but notice what the Hardy-Weinberg Equilibrium Law gives us: it outlines exactly what processes are essential to prevent evolution, and therefore by negation shows us how evolution can happen.

That is, if any of the five conditions for maintaining a Hardy-Weinberg equilibrium are not met, then evolution must be occurring. And, of course, virtually none of these conditions is ever permanently met in any known natural population of organisms:

• Mutations occur at a slow but steady rate in all known populations.

• Many organisms, especially animals, enter (immigration) and leave (emigration) populations.

• Most populations are not large enough to be unaffected by random changes in allele frequencies.

• Survival is virtually never random.

• Reproduction in organisms that can choose their mates is also virtually never random.

Therefore, according to the Hardy-Weinberg Equilibrium Law, evolution (defined as changes in allele frequencies over time) must be occurring in virtually every population of living organisms. In other words,

Evolution is as ubiquitous and inescapable as gravity.

THE MODERN EVOLUTIONARY SYNTHESIS

The Hardy-Weinberg Equilibrium Law provided more than just a "null hypothesis" for genetic evolution. It also provided a mathematical basis for a much more comprehensive theory of evolution now known as the modern evolutionary synthesis (often called "neo-darwinism"). During the 1930s and 40s, R. A. Fisher, J. B. S. Haldane, Sewall Wright, and Theodosius Dobzhansky developed mathematical models for fitness, selection, and other evolutionary processes. These models were then applied to demographic data derived from artificial and natural populations of organisms in a rigorous (and ongoing) series of empirical tests of the validity of the neo-darwinian model for genetic evolution. As a result of their work, Darwin's theories of natural and sexual selection were combined with Mendelian genetics, biometry and statistics, demography, paleontology, comparative anatomy, botany, and (more recently) molecular genetics and ethology to produce a "grand unified theory" of the origin and evolution of life on Earth.

The Genetical Theory of Natural Selection


Ronald Aylmer Fisher built on the pioneering theoretical work of Hardy, Weinberg, and Castle by providing mathematical models that further undermined the Mendelian geneticist's theory of evolution via mutation. He did this by showing that continuous variation could provide the basis for natural selection as proposed by Darwin. In his most important work, The Genetical Theory of Natural Selection (published in 1930) Fisher showed that traits characterized by continuous variation (i.e. those that approximate a normal, or bell-shaped, distribution) were both common and could provide all the raw material necessary for Darwinian natural selection. This is because such traits, although being continuous in populations, do not blend from parents to offspring. Instead, as Mendel first showed, they are produced by unblending "particles" of inheritance (i.e. Mendelian "genes"). In other words,

Mendelian inheritance conserves, rather than eventually destroying, the genetic variation that exists in natural populations.

Fisher is perhaps best known for what he called the Fundamental Theorem of Natural Selection. Using a series of essentially mathematical arguments, Fisher showed that the rate of change via natural selection was a direct function of the amount of variation in a population. That is,

The more variation among alleles that exists in a population, the faster natural selection can causes changes in the allele frequencies in that population.

Conversely, the less variation among alleles that exists in a population, the slower natural selection can causes changes in the allele frequencies in that population.

R. A. Fisher's work formed the basis for a mathematical theory of evolution in which the process of natural selection is modeled mathematically in the same way that Newton modeled the force of gravity. Indeed, Fisher pointed out several times that the mathematics of natural selection were similar in many ways to such physical models as the ideal gas laws and the second law of thermodynamics. According to his mathematical models, alleles that were positively selected would increase in frequency in populations in much the same was as gas molecules spread out in an expanding balloon.

To many evolutionary biologists, this meant that natural selection would inevitably result in "fixation" of alleles that were not selected against. That is,

Any allele that results in increased survival and reproduction should, if given enough time, eventually become the only allele for that particular trait in a particular population.

This presented a problem to evolutionary biologists that was almost as severe as the “mutationism” of the early Mendelians. It implied that the inevitable result of natural selection would be the eventual elimination of all non-adaptive variation in natural populations. This would then cause natural selection to grind to a halt (or to become reduced to essentially the rate of production of new genetic mutations, which is slow in the extreme, much slower than the observed rate of evolution). Fisher suggested that constant environmental change would cause different alleles to be selected for and against, and that therefore fixation might not ever happen. However, this argument seemed to be "tacked on" to his argument for the relationship between the amount of variation in populations and the speed of evolutionary change via natural selection.

Adaptive Landscapes and Genetic Drift


A solution to this problem was provided by Sewall Wright, who discovered a process that has eventually become known as genetic drift. Wright, who worked primarily with domesticated animals in controlled breeding programs, proposed that in small populations of organisms, random sampling errors could cause significant changes in allele frequencies in those populations. He showed mathematically that the smaller a population was, the greater the effect of such random events on its allele frequencies. In other words,

Evolution can proceed by at least three primary mechanisms: natural selection, sexual selection, and random genetic drift.

Wright's discovery of genetic drift solved the problem that Fisher's Fundamental Theorem posed: how can natural selection be prevented from shutting itself down as the result of fixation? Wright proposed that allele frequencies could be visualized as forming what he came to call an "adaptive landscape". In an adaptive landscape, allele frequencies formed a series of hills and valleys, in which the top of a hill represented the highest an allele frequency could reach via natural selection. According to Fisher, there is an iron-clad rule operating here: if an allele is on a slope, it can only go up the slope via natural selection.


But this means "you can't get there from here": if a trait is at the top of one adaptive peak, it can't go down through a valley to get to the top of another, even higher (i.e. more adaptive) peak. What Wright showed was that "you can get there from here" if you drift there. That is, if a population becomes very small, it is possible for it to "drift" from one adaptive peak to another, without sliding down into the valley in between. This means that natural selection doesn't get "stuck"; populations at one adaptive peak can make it to another, even higher adaptive peak, so long as they drift randomly to it.

The Causes of Evolution


John Burdon Sanderson Haldane (usually referred to as J. B. S. Haldane) solidified the revolution in theoretical population genetics begun by Hardy, Weinberg, Castle, Fisher, and Wright. In his most important book, The Causes of Evolution, published in 1932, he showed that genetic mutations could provide the raw material for Darwinian natural selection. Furthermore, he showed mathematically that such mutations could do this even when their frequency in a population was initially so low that they would be "invisible" to statistical analysis. He also showed how dominance could evolve in populations by means of natural selection, even when the original expression of an allele was initially recessive.

Haldane is also remembered for two quips that are often repeated by evolutionary biologists. The first concerns a question posed to him by an Anglican minister, who asked him (supposedly at a dinner party) what his study of nature had led him to conclude about the principle concern of the Creator. Without batting an eyelash, Haldane replied: "An inordinate fondness for beetles," referring to the fact that there are more species of beetles on Earth than any other kind of organism.

During another conversation (supposedly in a pub), Haldane was confronted with the observation that natural selection should result in pure selfishness on the part of individuals, and therefore no one should be willing to risk his own life to save another. To this Haldane replied,

"I would be willing to risk my life to save two brothers or eight cousins."

This quip is based upon the observation that brothers share an average of one-half of their genetic material, whereas first cousins share an average of one-eighth. Therefore, saving two brothers or four cousins would result in the same genetic contribution to the next generation as that represented by one's own genome. This quip was later cited by one of the founders of what is now know as the theory of kin selection in which natural selection is considered to act at the level of genes, rather than individuals. I will discuss this idea in more detail in a later blog post.

R. A. Fisher, J. B. S. Haldane, and Sewall Wright are usually recognized as having laid the theoretical foundation for modern evolutionary theory. However, many evolutionary biologists and historians of science consider that the "modern evolutionary synthesis” was initiated by Theodosius Dobzhansky with the publication of his most famous book, Genetics and the Origin of Species published in 1937.

Genetics and the Origin of Species


Dobzhansky combined the Mendelian genetics, the mathematical models of Fisher, Haldane, and Wright, and the observations of evolution and natural selection in the wild in a theory that reinstated natural selection as the primary engine of evolution. He emphasized both the scientific aspects of evolutionary theory, and the implications of evolutionary theory for education and society in general. In a famous essay entitled "Nothing in biology makes sense except in the light of evolution” he showed how modern synthetic evolutionary theory provides a comprehensive explanation for the origin and evolution of life on Earth.

Dobzhansky also grounded the "modern evolutionary synthesis" in empirical investigation. Using the common fruit fly (Drosophila melanogaster). Dobzhansky and his colleagues showed that the patterns of variation and natural selection predicted by Fisher actually occurred in controlled populations of living organisms under laboratory conditions.


Most importantly, Dobzhansky showed empirically that the "continuous variation" that both Darwin and Fisher asserted were essential for natural selection actually occurred for many traits in nature. According to Dobzhansky, most traits are distributed in what is often referred to as a "bell-shaped curve". That is, for most traits there is an average value for the trait, which the majority of the members of the population share. There is also two "tails" to the bell-shaped curve, consisting of extreme versions of the trait.

Dobzhansky then went on to identify three different forms of natural selection, which depended upon which part of the bell-shaped curve of variation selection affected:


• Directional selection, in which selection against one extreme "tail" of the bell-shaped curve caused the average value for the trait to move over time;


• Stabilizing selection, in which selection against both extreme "tails" of the bell-shaped curve caused the average value for the trait to remain where it was; and


• Disruptive selection, in which selection against the average value of the bell-shaped curve caused the population to split into two diverging curves, corresponding to the two extreme versions of the trait.

The proponents of the "modern evolutionary synthesis" asserted that this last form of natural selection was the underlying explanation for the divergence of one species into two or more different species (for this reason, disruptive selection is sometimes referred to as "diversifying selection"). That is, Darwin's "mystery of mysteries" – the origin of species – was shown to have a mathematical basis which could be studied empirically and tested statistically, thereby making it a genuinely "scientific" study.

The Historical Importance of the "Modern Evolutionary Synthesis"

What, then, was the importance of the “modern evolutionary synthesis” to evolutionary theory? Perhaps J.B.S. Haldane said it best:

"The permeation of biology by mathematics is only beginning, but unless the history of science is an inadequate guide, it will continue, and the investigations here summarized represent the beginning of a new branch of applied mathematics."

The theory of evolution as Darwin first proposed it was essentially a qualitative theory; it had no mathematical basis, and could not be tested using statistical methods. Indeed, Darwin himself was a “mathophobe,” who had neither the training nor the inclination to provide a mathematical basis for his theories.

However, the founders of the modern synthesis were all well-versed in mathematics, as was Gregor Mendel. Indeed, R. A. Fisher not only provided the first solid mathematical framework for the theory of evolution by natural selection, he virtually founded the disciplines of biometry and statistics. Many of the statistical tests that are still used to test evolutionary hypotheses (indeed, hypotheses throughout the natural and social sciences) were first formulated by Fisher.

Providing a mathematical foundation for evolutionary theory literally meant converting evolution from “natural history” into a modern science. When a hypothesis can be tested by gathering numerical data (by counting or measuring objects and events), that data can then be statistically tested to determine if it verifies or falsifies that hypothesis. This is what happens in the other natural sciences, like chemistry and physics. Since the modern evolutionary synthesis, this is also what happens in evolutionary biology.

ESSENTIAL READING:

Mayr, Ernst & William Provine (eds.) (1998) The Evolutionary Synthesis: Perspectives on the Unification of Biology. Harvard University Press.

SUPPLEMENTAL READING:

Bowler, Peter J. (1983) The Eclipse of Darwinism: Anti-Darwinian Evolutionary Theories in the Decades Around 1900. The Johns Hopkins University Press.

Darwin, Charles (1868) The Variation of Animals and Plants Under Domestication. John Murray. Available online here.

Dobzhansky, Theodosius (1937) Genetics and the Origin of Species. Columbia University Press.

Dobzhansky, Theodosius (1973) Nothing in biology makes sense except in the light of evolution. The American Biology Teacher, March 1973, volume 35, pages 125-129. Available online here.

Fisher, R. A. (1930) The Genetical Theory of Natural Selection. Oxford University Press.

Haldane, J. B. S. (1932) The Causes of Evolution. Princeton University Press.

Jenkin, Fleeming (1867). [Review of] The Origin of Species. The North British Review, June 1867, 46, pp. 277-318. Available online here.

Mendel, Gregor (1866) Experiments in Plant Hybridization. Verhandlungen des naturforschenden Vereines in Brünn, volume 4, pages 3-47. Available (in English) online here.

Provine, W. (1971) The Origins of Theoretical Population Genetics. University of Chicago Press.

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As always, comments, criticisms, and suggestions are warmly welcomed!

--Allen

Macroevolution: Examples and Evidence

AUTHOR: Allen MacNeill

SOURCE:
Observed Instances of Speciation

COMMENTARY: That's up to you...

In honor of Darwin’s birthday, here is a response to yet another unsupported assertion by creationists and ID supporters, who often state (without evidence) that although microevolution might happen, there is no evidence for macroevolution.

The distinction between microevolution – the mechanisms by which evolution has occurred – and
macroevolution – the large-scale pattern of change over time that has resulted from the operation of microevolutionary mechanisms – is as old as evolutionary theory. In the Origin of Species, Darwin himself argued for both microevolution (i.e. natural and sexual selection) and macroevolution (descent with modification), without using these terms. Following the publication of the Origin, Darwin’s theory of descent with modification was quickly accepted by virtually the entire scientific community. However, his proposed mechanisms of natural and sexual selection were not as widely accepted as the “engines” of descent with modification, falling into disrepute by the turn of the 20th century.

However, the founders of the “modern evolutionary synthesis” rehabilitated Darwin’s microevolutionary mechanisms by integrating them with Mendel’s theory of genetics and new discoveries in botany, ecology, ethology, historical geology, and paleontology. So successful was this synthesis that today all but the most committed young-Earth creationists accept that microevolution happens. However, it has become an article of faith among anti-evolutionists of all denominations, including “intelligent design” supporters, that there is no scientific explanation for macroevolution, and that in the case of the origin of humans, it didn’t happen.

There isn’t enough room in this post to address both of these misconceptions, so I will concentrate here on the first: that there is no evidence that macroevolution has happened, and that therefore it didn’t happen (or if it did, it required supernatural intervention). What follows is a brief sample of some examples of macroevolution and the mechanisms by which they have taken place, from the level of species up to the level of whole kingdoms. This is not an exhaustive sample by any means. However, it should give anyone with an open mind enough examples and evidence to form their own conclusions about the validity of modern macroevolutionary theory.

[I am particularly indebted to Joseph Boxhorn’s essay on the evidences for speciation (located at talk.origins.org) from which I have drawn many of these examples. Please go there to read more about them.]

MACROEVOLUTION AT THE LEVEL OF SPECIES

PLANTS


While studying the genetics of the evening primrose, Oenothera lamarckiana, de Vries (1905) found an unusual variant among his plants. Oenothera lamarckiana has a chromosome number of 2N = 14. The variant had a chromosome number of 2N = 28. He found that he was unable to breed this variant with Oenothera lamarckiana. He named this new species Oenothera gigas.


Digby (1912) crossed the primrose species Primula verticillata and Primula floribunda to produce a sterile hybrid. Polyploidization occurred in a few of these plants to produce fertile offspring. The new species was named Primula kewensis. Newton and Pellew (1929) note that spontaneous hybrids of Primula verticillata and Primula floribunda set tetraploid seed on at least three occasions. These happened in 1905, 1923 and 1926.


Owenby (1950) demonstrated that two species in the genus Tragopogon were produced by polyploidization from hybrids. He showed that Tragopogon miscellus found in a colony in Moscow, Idaho was produced by hybridization of Tragopogon dubius and Tragopogon pratensis. He also showed that Tragopogon mirus found in a colony near Pullman, Washington was produced by hybridization of Tragopogon dubius and Tragopogon porrifolius. Evidence from chloroplast DNA suggests that Tragopogon mirus has originated independently by hybridization in eastern Washington and western Idaho at least three times (Soltis and Soltis 1989). The same study also shows multiple origins for Tragopogon micellus.


The Russian cytologist Karpchenko (1927, 1928) crossed the radish, Raphanus sativus, with the cabbage, Brassica oleracea. Despite the fact that the plants were in different genera, he got a sterile hybrid. Some unreduced gametes were formed in the hybrids. This allowed for the production of seed. Plants grown from the seeds were interfertile with each other. They were not interfertile with either parental species. Unfortunately the new plant (genus Raphanobrassica) had the foliage of a radish and the root of a cabbage.


A species of hemp nettle, Galeopsis tetrahit, was hypothesized to be the result of a natural hybridization of two other species, Galeopsis pubescens and Galeopsis speciosa (Muntzing 1932). The two species were crossed. The hybrids matched Galeopsis tetrahit in both visible features and chromosome morphology.


Clausen et al. (1945) hypothesized that Madia citrigracilis was a hexaploid hybrid of Madia gracilis and Madia citriodora. As evidence they noted that the species have gametic chromosome numbers of n = 24, 16 and 8 respectively. Crossing Madia gracilis and Madia citriodora resulted in a highly sterile triploid with n = 24. The chromosomes formed almost no bivalents during meiosis. Artificially doubling the chromosome number using colchecine produced a hexaploid hybrid which closely resembled Madia citrigracilis and was fertile.


Frandsen (1943, 1947) showed that Brassica carinata (n = 17) may be recreated by hybridizing Brassica nigra (n = 8) and Brassica oleracea, Brassica juncea (n = 18) may be recreated by hybridizing Brassica nigra and Brassica campestris (n = 10), and Brassica napus (n = 19) may be recreated by hybridizing Brassica oleracea and Brassica campestris.


Rabe and Haufler (1992) found a naturally occurring diploid sporophyte of maidenhair fern (Adiantum pedatum) which produced unreduced (2N) spores. These spores resulted from a failure of the paired chromosomes to dissociate during the first division of meiosis. The spores germinated normally and grew into diploid gametophytes. These did not appear to produce antheridia. Nonetheless, a subsequent generation of tetraploid sporophytes was produced. When grown in the lab, the tetraploid sporophytes appear to be less vigorous than the normal diploid sporophytes. The 4N individuals were found near Baldwin City, Kansas.


Woodsia Fern (Woodsia abbeae) was described as a hybrid of Woodsia cathcariana and Woodsia ilvensis (Butters 1941). Plants of this hybrid normally produce abortive sporangia containing inviable spores. In 1944 Butters found a Woodsia abbeae plant near Grand Portage, Minn. that had one fertile frond (Butters and Tryon 1948). The apical portion of this frond had fertile sporangia. Spores from this frond germinated and grew into prothallia. About six months after germination sporophytes were produced. They survived for about one year. Based on cytological evidence, Butters and Tryon concluded that the frond that produced the viable spores had gone tetraploid. They made no statement as to whether the sporophytes grown produced viable spores.


Gottlieb (1973) documented the speciation of Stephanomeria malheurensis. He found a single small population (< 250 plants) among a much larger population (> 25,000 plants) of Stephanomeria exigua in Harney Co., Oregon. Both species are diploid and have the same number of chromosomes (N = 8). Stephanomeria exigua is an obligate outcrosser exhibiting sporophytic self-incompatibility. Stephanomeria malheurensis exhibits no self-incompatibility and self-pollinates. Though the two species look very similar, Gottlieb was able to document morphological differences in five characters plus chromosomal differences. F1 hybrids between the species produces only 50% of the seeds and 24% of the pollen that conspecific crosses produced. F2 hybrids showed various developmental abnormalities.


Pasterniani (1969) produced almost complete reproductive isolation between two varieties of maize (Zea mays). The varieties were distinguishable by seed color, white versus yellow. Other genetic markers allowed him to identify hybrids. The two varieties were planted in a common field. Any plant's nearest neighbors were always plants of the other strain. Selection was applied against hybridization by using only those ears of corn that showed a low degree of hybridization as the source of the next years seed. Only parental type kernels from these ears were planted. The strength of selection was increased each year. In the first year, only ears with less than 30% intercrossed seed were used. In the fifth year, only ears with less than 1% intercrossed seed were used. After five years the average percentage of intercrossed matings dropped from 35.8% to 4.9% in the white strain and from 46.7% to 3.4% in the yellow strain.


At reasonably low concentrations, copper is toxic to many plant species. However, several plants have been seen to develop a tolerance to this metal (Macnair 1981). Macnair and Christie (1983) used this to examine the genetic basis of a postmating isolating mechanism in yellow monkey flower (Mimulus guttatus). When they crossed plants from the copper tolerant "Copperopolis" population with plants from the nontolerant "Cerig" population, they found that many of the hybrids were inviable. During early growth, just after the four leaf stage, the leaves of many of the hybrids turned yellow and became necrotic. Death followed this. This was seen only in hybrids between the two populations. Through mapping studies, the authors were able to show that the copper tolerance gene and the gene responsible for hybrid inviability were either the same gene or were very tightly linked. These results suggest that reproductive isolation may require changes in only a small number of genes.

ANIMALS

Speciation through hybridization and/or polyploidy is now considered to be as important in animals as it is in plants. (Lokki and Saura 1980; Bullini and Nascetti 1990; Vrijenhoek 1994). Bullini and Nasceti (1990) review chromosomal and genetic evidence that suggest that speciation through hybridization may occur in a number of insect species, including walking sticks, grasshoppers, blackflies and cucurlionid beetles. Lokki and Saura (1980) discuss the role of polyploidy in insect evolution. Vrijenhoek (1994) reviews the literature on parthenogenesis and hybridogenesis in fish.

Dobzhansky and Pavlovsky (1971) reported a speciation event that occurred in a laboratory culture of Drosophila paulistorum sometime between 1958 and 1963. The culture was descended from a single inseminated female that was captured in the Llanos of Colombia. In 1958 this strain produced fertile hybrids when crossed with conspecifics of different strains from Orinocan. From 1963 onward crosses with Orinocan strains produced only sterile males. Initially no assortative mating or behavioral isolation was seen between the Llanos strain and the Orinocan strains. Later on Dobzhansky produced assortative mating (Dobzhansky 1972).


Thoday and Gibson (1962) established a population of Drosophila melanogaster from four gravid females. They applied selection on this population for flies with the highest and lowest numbers of sternoplural chaetae (hairs). In each generation, eight flies with high numbers of chaetae were allowed to interbreed and eight flies with low numbers of chaetae were allowed to interbreed. Periodically they performed mate choice experiments on the two lines. They found that they had produced a high degree of positive assortative mating between the two groups. In the decade or so following this, eighteen labs attempted unsuccessfully to reproduce these results. References are given in Thoday and Gibson 1970.

Crossley (1974) was able to produce changes in mating behavior in two mutant strains of Drosophila melanogaster. Four treatments were used. In each treatment, 55 virgin males and 55 virgin females of both ebony body mutant flies and vestigial wing mutant flies (220 flies total) were put into a jar and allowed to mate for 20 hours. The females were collected and each was put into a separate vial. The phenotypes of the offspring were recorded. Wild type offspring were hybrids between the mutants. In two of the four treatments, mating was carried out in the light. In one of these treatments all hybrid offspring were destroyed. This was repeated for 40 generations. Mating was carried out in the dark in the other two treatments. Again, in one of these all hybrids were destroyed. This was repeated for 49 generations. Crossley ran mate choice tests and observed mating behavior. Positive assortative mating was found in the treatment which had mated in the light and had been subject to strong selection against hybridization. The basis of this was changes in the courtship behaviors of both sexes. Similar experiments, without observation of mating behavior, were performed by Knight, et al. (1956).

Kilias, et al. (1980) exposed Drosophila melanogaster populations to different temperature and humidity regimes for several years. They performed mating tests to check for reproductive isolation. They found some sterility in crosses among populations raised under different conditions. They also showed some positive assortative mating. These things were not observed in populations which were separated but raised under the same conditions. They concluded that sexual isolation was produced as a byproduct of selection.

In a series of papers (Rice 1985, Rice and Salt 1988 and Rice and Salt 1990) Rice and Salt presented experimental evidence for the possibility of sympatric speciation in Drosophila melanogaster. They started from the premise that whenever organisms sort themselves into the environment first and then mate locally, individuals with the same habitat preferences will necessarily mate assortatively. They established a stock population of Drosophila melanogaster with flies collected in an orchard near Davis, California. Pupae from the culture were placed into a habitat maze. Newly emerged flies had to negotiate the maze to find food. The maze simulated several environmental gradients simultaneously. The flies had to make three choices of which way to go. The first was between light and dark (phototaxis). The second was between up and down (geotaxis). The last was between the scent of acetaldehyde and the scent of ethanol (chemotaxis). This divided the flies among eight habitats. The flies were further divided by the time of day of emergence. In total the flies were divided among 24 spatio-temporal habitats.

They next cultured two strains of flies that had chosen opposite habitats. One strain emerged early, flew upward and was attracted to dark and acetaldehyde. The other emerged late, flew downward and was attracted to light and ethanol. Pupae from these two strains were placed together in the maze. They were allowed to mate at the food site and were collected. Eye color differences between the strains allowed Rice and Salt to distinguish between the two strains. A selective penalty was imposed on flies that switched habitats. Females that switched habitats were destroyed. None of their gametes passed into the next generation. Males that switched habitats received no penalty. After 25 generations of this mating tests showed reproductive isolation between the two strains. Habitat specialization was also produced.

They next repeated the experiment without the penalty against habitat switching. The result was the same -- reproductive isolation was produced. They argued that a switching penalty is not necessary to produce reproductive isolation. Their results, they stated, show the possibility of sympatric speciation.


In a series of experiments, del Solar (1966) derived positively and negatively geotactic and phototactic strains of Drosophila pseudoobscura from the same population by running the flies through mazes. Flies from different strains were then introduced into mating chambers (10 males and 10 females from each strain). Matings were recorded. Statistically significant positive assortative mating was found.

In a separate series of experiments Dodd (1989) raised eight populations derived from a single population of Drosophila pseudoobscura on stressful media. Four populations were raised on a starch based medium, the other four were raised on a maltose based medium. The fly populations in both treatments took several months to get established, implying that they were under strong selection. Dodd found some evidence of genetic divergence between flies in the two treatments. He performed mate choice tests among experimental populations. He found statistically significant assortative mating between populations raised on different media, but no assortative mating among populations raised within the same medium regime. He argued that since there was no direct selection for reproductive isolation, the behavioral isolation results from a pleiotropic by-product to adaptation to the two media. Schluter and Nagel (1995) have argued that these results provide experimental support for the hypothesis of parallel speciation.


Less dramatic results were obtained by growing Drosophila willistoni on media of different pH levels (de Oliveira and Cordeiro 1980). Mate choice tests after 26, 32, 52 and 69 generations of growth showed statistically significant assortative mating between some populations grown in different pH treatments. This ethological isolation did not always persist over time. They also found that some crosses made after 106 and 122 generations showed significant hybrid inferiority, but only when grown in acid medium.

Some proposed models of speciation rely on a process called reinforcement to complete the speciation process. Reinforcement occurs when to partially isolated allopatric populations come into contact. Lower relative fitness of hybrids between the two populations results in increased selection for isolating mechanisms. I should note that a recent review (Rice and Hostert 1993) argues that there is little experimental evidence to support reinforcement models. Two experiments in which the authors argue that their results provide support are discussed below.

Ehrman (1971) established strains of wild-type and mutant (black body) Drosophila melanogaster. These flies were derived from compound autosome strains such that heterotypic matings would produce no progeny. The two strains were reared together in common fly cages. After two years, the isolation index generated from mate choice experiments had increased from 0.04 to 0.43, indicating the appearance of considerable assortative mating. After four years this index had risen to 0.64 (Ehrman 1973). Along the same lines, Koopman (1950) was able to increase the degree of reproductive isolation between two partially isolated species, Drosophila pseudoobscura and Drosophila persimilis.

The founder-flush (a.k.a. flush-crash) hypothesis posits that genetic drift and founder effects play a major role in speciation (Powell 1978). During a founder-flush cycle a new habitat is colonized by a small number of individuals (e.g. one inseminated female). The population rapidly expands (the flush phase). This is followed by the population crashing. During this crash period the population experiences strong genetic drift. The population undergoes another rapid expansion followed by another crash. This cycle repeats several times. Reproductive isolation is produced as a byproduct of genetic drift.

Dodd and Powell (1985) tested this hypothesis using Drosophila pseudoobscura. A large, heterogeneous population was allowed to grow rapidly in a very large population cage. Twelve experimental populations were derived from this population from single pair matings. These populations were allowed to flush. Fourteen months later, mating tests were performed among the twelve populations. No postmating isolation was seen. One cross showed strong behavioral isolation. The populations underwent three more flush-crash cycles. Forty-four months after the start of the experiment (and fifteen months after the last flush) the populations were again tested. Once again, no postmating isolation was seen. Three populations showed behavioral isolation in the form of positive assortative mating. Later tests between 1980 and 1984 showed that the isolation persisted, though it was weaker in some cases.

Galina, et al. (1993) performed similar experiments with Drosophila pseudoobscura. Mating tests between populations that underwent flush-crash cycles and their ancestral populations showed 8 cases of positive assortative mating out of 118 crosses. They also showed 5 cases of negative assortative mating (i.e. the flies preferred to mate with flies of the other strain). Tests among the founder-flush populations showed 36 cases of positive assortative mating out of 370 crosses. These tests also found 4 cases of negative assortative mating. Most of these mating preferences did not persist over time. Galina, et al. concluded that the founder-flush protocol yields reproductive isolation only as a rare and erratic event.

Ahearn (1980) applied the founder-flush protocol to Drosophila silvestris. Flies from a line of this species underwent several flush-crash cycles. They were tested in mate choice experiments against flies from a continuously large population. Female flies from both strains preferred to mate with males from the large population. Females from the large population would not mate with males from the founder flush population. An asymmetric reproductive isolation was produced.

In a three year experiment, Ringo, et al. (1985) compared the effects of a founder-flush protocol to the effects of selection on various traits. A large population of Drosophila simulans was created from flies from 69 wild caught stocks from several locations. Founder-flush lines and selection lines were derived from this population. The founder-flush lines went through six flush-crash cycles. The selection lines experienced equal intensities of selection for various traits. Mating test were performed between strains within a treatment and between treatment strains and the source population. Crosses were also checked for postmating isolation. In the selection lines, 10 out of 216 crosses showed positive assortative mating (2 crosses showed negative assortative mating). They also found that 25 out of 216 crosses showed postmating isolation. Of these, 9 cases involved crosses with the source population. In the founder-flush lines 12 out of 216 crosses showed positive assortative mating (3 crosses showed negative assortative mating). Postmating isolation was found in 15 out of 216 crosses, 11 involving the source population. They concluded that only weak isolation was found and that there was little difference between the effects of natural selection and the effects of genetic drift.


Meffert and Bryant (1991) used houseflies (Musca domestica) to test whether bottlenecks in populations can cause permanent alterations in courtship behavior that lead to premating isolation. They collected over 100 flies of each sex from a landfill near Alvin, Texas. These were used to initiate an ancestral population. From this ancestral population they established six lines. Two of these lines were started with one pair of flies, two lines were started with four pairs of flies and two lines were started with sixteen pairs of flies. These populations were flushed to about 2,000 flies each. They then went through five bottlenecks followed by flushes. This took 35 generations. Mate choice tests were performed. One case of positive assortative mating was found. One case of negative assortative mating was also found.

Soans, et al. (1974) used houseflies (Musca domestica) to test Pimentel's model of speciation. This model posits that speciation requires two steps. The first is the formation of races in subpopulations. This is followed by the establishment of reproductive isolation. Houseflies were subjected to intense divergent selection on the basis of positive and negative geotaxis. In some treatments no gene flow was allowed, while in others there was 30% gene flow. Selection was imposed by placing 1000 flies into the center of a 108 cm vertical tube. The first 50 flies that reached the top and the first 50 flies that reached the bottom were used to found positively and negatively geotactic populations. Four populations were established:

Population A: positive geotaxis, no gene flow
Population B: negative geotaxis, no gene flow
Population C: positive geotaxis, 30% gene flow
Population D: negative geotaxis, 30% gene flow

Selection was repeated within these populations each generations. After 38 generations the time to collect 50 flies had dropped from 6 hours to 2 hours in Pop A, from 4 hours to 4 minutes in Pop B, from 6 hours to 2 hours in Pop C and from 4 hours to 45 minutes in Pop D. Mate choice tests were performed. Positive assortative mating was found in all crosses. They concluded that reproductive isolation occurred under both allopatric and sympatric conditions when very strong selection was present. Hurd and Eisenberg (1975) performed a similar experiment on houseflies using 50% gene flow and got the same results.

Recently there has been a lot of interest in whether the differentiation of an herbivorous or parasitic species into races living on different hosts can lead to sympatric speciation. It has been argued that in animals that mate on (or in) their preferred hosts, positive assortative mating is an inevitable byproduct of habitat selection (Rice 1985; Barton, et al. 1988). This would suggest that differentiated host races may represent incipient species.


The Apple Maggot Fly (Rhagoletis pomonella) is a fly that is native to North America. Its normal host is the hawthorn tree (Crataegus monogyna). Sometime during the nineteenth century it began to infest apple trees. Since then it has begun to infest cherries, roses, pears and possibly other members of the Rosaceae. Quite a bit of work has been done on the differences between flies infesting hawthorn and flies infesting apple. There appear to be differences in host preferences among populations. Offspring of females collected from on of these two hosts are more likely to select that host for oviposition (Prokopy et al. 1988). Genetic differences between flies on these two hosts have been found at 6 out of 13 allozyme loci (Feder et al. 1988, see also McPheron et al. 1988). Laboratory studies have shown an asynchrony in emergence time of adults between these two host races (Smith 1988). Flies from apple trees take about 40 days to mature, whereas flies from hawthorn trees take 54-60 days to mature. This makes sense when we consider that hawthorn fruit tends to mature later in the season that apples. Hybridization studies show that host preferences are inherited, but give no evidence of barriers to mating. This is a very exciting case. It may represent the early stages of a sympatric speciation event (considering the dispersal of Rhagoletis pomonella to other plants it may even represent the beginning of an adaptive radiation). It is important to note that some of the leading researchers on this question are urging caution in interpreting it. Feder and Bush (1989) stated:

"Hawthorn and apple "host races" of Rhagoletis pomonella may therefore represent incipient species. However, it remains to be seen whether host-associated traits can evolve into effective enough barriers to gene flow to result eventually in the complete reproductive isolation of Rhagoletis pomonella populations."

Gall Former Fly (Eurosta solidaginis) is a gall forming fly that is associated with goldenrod ( Solidago sp.) plants. It has two hosts: over most of its range it lays its eggs in Solidago altissima, but in some areas it uses Solidago gigantea as its host. Recent electrophoretic work has shown that the genetic distances among flies from different sympatric hosts species are greater than the distances among flies on the same host in different geographic areas (Waring et al. 1990). This same study also found reduced variability in flies on Solidago gigantea. This suggests that some Eurosta solidaginis have recently shifted hosts to this species. A recent study has compared reproductive behavior of the flies associated with the two hosts (Craig et al. 1993). They found that flies associated with Solidago gigantea emerge earlier in the season than flies associated with Solidago altissima. In host choice experiments, each fly strain ovipunctured its own host much more frequently than the other host.

Craig et al. (1993) also performed several mating experiments. When no host was present and females mated with males from either strain, if males from only one strain were present. When males of both strains were present, statistically significant positive assortative mating was seen. In the presence of a host, assortative mating was also seen. When both hosts and flies from both populations were present, females waited on the buds of the host that they are normally associated with. The males fly to the host to mate. This may represent the beginning of a sympatric speciation.


Halliburton and Gall (1981) established a population of flour beetles (Tribolium castaneum) collected in Davis, California. In each generation they selected the 8 lightest and the 8 heaviest pupae of each sex. When these 32 beetles had emerged, they were placed together and allowed to mate for 24 hours. Eggs were collected for 48 hours. The pupae that developed from these eggs were weighed at 19 days. This was repeated for 15 generations. The results of mate choice tests between heavy and light beetles was compared to tests among control lines derived from randomly chosen pupae. Positive assortative mating on the basis of size was found in 2 out of 4 experimental lines.


In 1964 five or six individuals of the polychaete worm, Nereis acuminata, were collected in Long Beach Harbor, California. These were allowed to grow into a population of thousands of individuals. Four pairs from this population were transferred to the Woods Hole Oceanographic Institute. For over 20 years these worms were used as test organisms in environmental toxicology. From 1986 to 1991 the Long Beach area was searched for populations of the worm. Two populations, P1 and P2, were found. Weinberg, et al. (1992) performed tests on these two populations and the Woods Hole population (WH) for both postmating and premating isolation. To test for postmating isolation, they looked at whether broods from crosses were successfully reared. The results below give the percentage of successful rearings for each group of crosses.

WH × WH = 75%
P1 × P1 = 95%
P2 × P2 = 80%
P1 × P2 = 77%
WH × P1 = 0%
WH × P2 = 0%

They also found statistically significant premating isolation between the WH population and the field populations. Finally, the Woods Hole population showed slightly different karyotypes from the field populations.

In some species the presence of intracellular bacterial parasites (or symbionts) is associated with postmating isolation. This results from a cytoplasmic incompatability between gametes from strains that have the parasite (or symbiont) and stains that don't. An example of this is seen in the mosquito Culex pipiens (Yen and Barr 1971). Compared to within strain matings, matings between strains from different geographic regions may may have any of three results: These matings may produce a normal number of offspring, they may produce a reduced number of offspring or they may produce no offspring. Reciprocal crosses may give the same or different results. In an incompatible cross, the egg and sperm nuclei fail to unite during fertilization. The egg dies during embryogenesis. In some of these strains, Yen and Barr (1971) found substantial numbers of Rickettsia-like microbes in adults, eggs and embryos. Compatibility of mosquito strains seems to be correlated with the strain of the microbe present. Mosquitoes that carry different strains of the microbe exhibit cytoplasmic incompatibility; those that carry the same strain of microbe are interfertile.

Similar phenomena have been seen in a number of other insects. Microoganisms are seen in the eggs of both Nasonia vitripennis and Nasonia giraulti. These two species do not normally hybridize. Following treatment with antibiotics, hybrids occur between them (Breeuwer and Werren 1990). In this case, the symbiont is associated with improper condensation of host chromosomes. For more examples and a critical review of this topic, see Thompson 1987.

MACROEVOLUTION ABOVE THE LEVEL OF SPECIES


Boraas (1983) reported the induction of multicellularity in a strain of Chlorella pyrenoidosa (since reclassified as Chlorella vulgaris) by predation. He was growing the unicellular green alga in the first stage of a two stage continuous culture system as for food for a flagellate predator, Ochromonas sp., that was growing in the second stage. Due to the failure of a pump, flagellates washed back into the first stage. Within five days a colonial form of the Chlorella appeared. It rapidly came to dominate the culture. The colony size ranged from 4 cells to 32 cells. Eventually it stabilized at 8 cells. This colonial form has persisted in culture for about a decade. The new form has been keyed out using a number of algal taxonomic keys. They key out now as being in the genus Coelosphaerium, which is in a different family from Chlorella.

Shikano, et al. (1990) reported that an unidentified bacterium underwent a major morphological change when grown in the presence of a ciliate predator. This bacterium's normal morphology is a short (1.5 um) rod. After 8 - 10 weeks of growing with the predator it assumed the form of long (20 um) cells. These cells have no cross walls. Filaments of this type have also been produced under circumstances similar to Boraas' induction of multicellularity in Chlorella. Microscopic examination of these filaments is described in Gillott et al. (1993). Multicellularity has also been produced in unicellular bacterial by predation (Nakajima and Kurihara 1994). In this study, growth in the presence of protozoal grazers resulted in the production of chains of bacterial cells.


The “species flock” of over 600 species of cichlid fish in Lake Victoria have all diverged within the past 15,000 years, according to Tijs Goldschmidt. Lake Victoria, the source of the Nile River in east Africa, was formed by block faulting in the African great rift valley. Geological evidence indicates that the lake was originally formed about 400,000 years ago, but dried out about 15,000 years ago. It subsequently refilled, and the 600+ species of cichlid fish have adaptively radiated during that period of time.

As the lake constitutes a single, although very large ecosystem, the adaptive radiation of the cichlid fish of Lake Victoria must be considered to have undergone a massive sympatric divergence. That this is the case is further supported by the observation that the extraordinary phenotypic variation seen among these fish has been accompanied by almost no genetic variation, except for a very small number of homeotic genes. Goldschmidt has suggested that the adaptive radiation of the cichlids of Lake Victoria has been driven by a combination of adaptation to a myriad of trophic niches, combined with sexual selection resulting from female choice (Goldschmidt, 1998).

MACROEVOLUTION AT THE LEVEL OF KINGDOMS


In 1970, Lynn Margulis proposed that the four kingdoms of eukaryotes (Protoctista, Fungi, Plantae, and Animalia, now combined in the domain Eukarya) originated from the endosymbiotic combination of four prokaryotic (i.e. bacterial) ancestors. The first step in this endosymbiotic partnership was the endosymbiotic incorporation of an aerobic bacterium with an acid-tolerant (probably Archaean) prokaryotic ancestor. The aerobic bacterium eventually evolved into what we now recognize as mitochondria. That this was the first step in the endosymbiotic origin of eukaryotes is supported by the observation that all eukaryotic cells (except such specialized cells as erythrocytes) have mitochondria, indicating that bacteria-derived mitochondria became associated with the ancestors of eukaryotes prior to the splitting of the eukaryotic clade into the plant, fungus, and animal kingdoms.

Margulis cites several lines of evidence supporting the hypothesis that mitochondria originated as endosymbiotic aerobic bacteria:

• Mitochondria have a double membrane. The outer membrane is very similar to the membrane of the vacuoles of eukaryotic cells, while the inner membrane is much more similar to the plasma membrane of bacteria.

• Like bacteria, mitochondria have circular DNA molecules, whereas the DNA molecules in the nuclear chromosomes of eukaryotes is linear.

• Also like bacteria, the circular DNA molecules of mitochondria are not complexed with histone proteins, whereas the linear DNA molecules in the chromosomes of the eukaryotic nucleus are tightly complexed with histone proteins.

• The DNA molecules of mitochondria (like the DNA of bacteria) do not include intron sequences, whereas the DNA molecules in the chromosomes of the eukaryotic nucleus generally include at least one, and often many intron sequences.

• Most of the genetic components of the mitochondrial genome, including such genetic “machinery” as promoter sequences and terminator sequences, are coded in the same way as in bacteria, and are significantly different from the genetic “machinery” in the DNA in the chromosomes of the eukaryotic nucleus.

•Mitochondria have their own ribosomes, which are virtually identical with bacterial ribosomes, but very different in size and structure from the ribosomes in the cytosol of eukaryotic cells.

• Mitochondria reproduce independently inside their host cells via binary fission, the same mechanism by which other bacteria reproduce, and very different from the process of mitosis by which eukaryotic cells divide.

The second step in the endosymbiotic origin of eukaryotes was the incorporation of motile, microtubule-containing bacteria similar to spirochaete bacteria into the mitochondrion-containing eukaryotic ancestor. Margulis proposed that these bacteria evolved into the cilia and flagella of eukaryotic cells (called undulapodia), which eventually evolved into the mitotic spindle apparatus by which all eukaryotic cells divide. She predicted that the basal bodies of cilia and flagella would have their own DNA, a prediction that was verified by researchers who (ironically) were trying to disprove her hypothesis. Another observation supporting Margulis’s hypothesis about the endosymbiotic origin of undulapodia is the fact that, like mitochondria, cilia and flagella reproduce independently of the cells to which they are attached, via a mechanism similar to binary fission. That the incorporation of spirochaete-like bacteria into the ancestors of all eukaryotes was the second step in the endosymbiotic origin of eukaryotes is supported by the observation that almost all eukaryotic cells (except a few very primitive species) reproduce via mitosis, indicating again that the undulapodia-derived spindle apparatus became associated with the ancestors of eukaryotes prior to the splitting of the eukaryotic clade into the plant, fungus, and animal kingdoms.

The final step in the endosymbiotic origin of eukaryotes was the incorporation of photosynthetic bacteria similar to cyanobacteria into the mitochondria-and-undulapodia-containing eukaryotic ancestor. These photosynthetic bacteria evolved into the chloroplasts of eukaryotic algae and plants. Like mitochondria, chloroplasts have a number of structural and functional similarities to photosynthetic bacteria that point to their endosymbiotic origin:

• Like mitochondria, chloroplasts have a double membrane. The outer membrane is very similar to the membrane of the vacuoles of eukaryotic cells, while the inner membrane is much more similar to the plasma membrane of bacteria.

• Like bacteria and mitochondria, chloroplasts have circular DNA molecules, whereas the DNA molecules in the nuclear chromosomes of eukaryotes is linear.

• Also like bacteria and mitochondria, the circular DNA molecules of chloroplasts are not complexed with histone proteins, whereas the linear DNA molecules in the chromosomes of the eukaryotic nucleus are tightly complexed with histone proteins.

• The DNA molecules of chloroplasts (like the DNA of bacteria and mitochondria) do not include intron sequences, whereas the DNA molecules in the chromosomes of the eukaryotic nucleus generally include at least one, and often many intron sequences.

• Most of the genetic components of the chloroplast genome, including such genetic “machinery” as promoter sequences and terminator sequences, are coded in the same way as in bacteria, and are significantly different from the genetic “machinery” in the DNA in the chromosomes of the eukaryotic nucleus.

•Like mitochondria, chloroplasts have their own ribosomes, which are virtually identical with bacterial ribosomes, but very different in size and structure from the ribosomes in the cytosol of eukaryotic cells.

• Like mitochondria, chloroplasts reproduce independently inside their host cells via binary fission, the same mechanism by which other bacteria reproduce, and very different from the process of mitosis by which eukaryotic cells divide.

• If separated from their eukaryotic host cells, chloroplasts can grow and reproduce on their own, looking and acting for all the world like photosynthetic bacteria.

That this was the final step in the endosymbiotic origin of eukaryotes is supported by the observation that only plant cells (and some protists) have chloroplasts, indicating that bacteria-derived chloroplasts became associated with the ancestors of eukaryotes after to the splitting of the eukaryotic clade into the plant, fungus, and animal kingdoms. This suggestion is strengthened by recent research indicating that fungi and animals are more closely related to each other than either are to plants, indicating that the split between photosynthetic eukaryotes (i.e. algae and plants) and heterotrophic eukaryotes (i.e. fungi and animals) happened before the incorporation of endosymbiotic photosynthetic bacteria in the ancestors of algae and plants.

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As always, comments, criticisms, and suggestions are warmly welcomed!

--Allen