Adaptation

This article is about the evolutionary process. For other uses, see Adaptation (disambiguation).

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An adaptation in biology is a trait with a current functional role in the life history of an organism that is maintained and evolved by means of natural selection. An adaptation refers to both the current state of being adapted and to the dynamic evolutionary process that leads to the adaptation. Adaptations contribute to the fitness and survival of individuals. Organisms face a succession of environmental challenges as they grow and develop and are equipped with an adaptive plasticity as the phenotype of traits develop in response to the imposed conditions. The developmental norm of reaction for any given trait is essential to the concept of adaptation as it affords a kind of biological insurance or resilience to varying environments.

General principles

The significance of an adaptation can only be understood in relation to the total biology of the species.

— Julian Huxley^[1]

Adaptation is, first of all, a process, rather than a physical part of a body.^[2] An internal parasite (such as a fluke) can illustrate the distinction: such a parasite may have a very simple bodily structure, but nevertheless the organism is highly adapted to its specific environment. From this we see that adaptation is not just a matter of visible traits: in such parasites critical adaptations take place in the life-cycle, which is often quite complex.^[3] However, as a practical term, adaptation is often used for the product: those features of a species which result from the process. Many aspects of an animal or plant can be correctly called adaptations, though there are always some features whose function is in doubt. By using the term adaptation for the evolutionary process, and adaptive trait for the bodily part or function (the product), the two senses of the word may be distinguished.^[4][5][6][7]

Adaptation is one of the two main processes that explain the diverse species we see in biology, such as the different species of Darwin's finches. The other is speciation (species-splitting or cladogenesis), caused by geographical isolation or some other mechanism.^[8][9] A favourite example used today to study the interplay of adaptation and speciation is the evolution of cichlid fish in African lakes, where the question of reproductive isolation is much more complex.^[10][11]

Adaptation is not always a simple matter, where the ideal phenotype evolves for a given external environment. An organism must be viable at all stages of its development and at all stages of its evolution. This places constraints on the evolution of development, behaviour and structure of organisms. The main constraint, over which there has been much debate, is the requirement that each genetic and phenotypic change during evolution should be relatively small, because developmental systems are so complex and interlinked. However, it is not clear what "relatively small" should mean, for example polyploidy in plants is a reasonably common large genetic change.^[12] The origin of the symbiosis of multiple micro-organisms to form a eukaryota is a more exotic example.^[13]

All adaptations help organisms survive in their ecological niches.^[14] These adaptive traits may be structural, behavioral or physiological. Structural adaptations are physical features of an organism (shape, body covering, armament; and also the internal organization). Behavioural adaptations are composed of inherited behaviour chains and/or the ability to learn: behaviours may be inherited in detail (instincts), or a tendency for learning may be inherited (see neuropsychology). Examples: searching for food, mating, vocalizations. Physiological adaptations permit the organism to perform special functions (for instance, making venom, secreting slime, phototropism); but also more general functions such as growth and development, temperature regulation, ionic balance and other aspects of homeostasis. Adaptation, then, affects all aspects of the life of an organism.

Definitions

The following definitions are mainly due to Theodosius Dobzhansky.

1. Adaptation is the evolutionary process whereby an organism becomes better able to live in its habitat or habitats.^[15]

2. Adaptedness is the state of being adapted: the degree to which an organism is able to live and reproduce in a given set of habitats.^[16]

3. An adaptive trait is an aspect of the developmental pattern of the organism which enables or enhances the probability of that organism surviving and reproducing.^[17]

Adaptedness and fitness

Main article: Fitness (biology)

From the above definitions, it is clear that there is a relationship between adaptedness and fitness (a key population genetics concept). Differences in fitness between genotypes predict the rate of evolution by natural selection. Natural selection changes the relative frequencies of alternative phenotypes, insofar as they are heritable.^[18] Although the two are connected, the one does not imply the other: a phenotype with high adaptedness may not have high fitness. Dobzhansky mentioned the example of the Californian redwood, which is highly adapted, but a relict species in danger of extinction.^[15] Elliott Sober commented that adaptation was a retrospective concept since it implied something about the history of a trait, whereas fitness predicts a trait's future.^[19]p210

1. Relative fitness. The average contribution to the next generation by a genotype or a class of genotypes, relative to the contributions of other genotypes in the population.^[20]p552 This is also known as Darwinian fitness, selective coefficient, and other terms.

2. Absolute fitness. The absolute contribution to the next generation by a genotype or a class of genotypes. Also known as the Malthusian parameter when applied to the population as a whole.^[18]

3. Adaptedness. The extent to which a phenotype fits its local ecological niche. This can sometimes be tested through a reciprocal transplant experiment.

Brief history

Main article: History of evolutionary thought

Adaptation as a fact of life has been accepted by all the great thinkers who have tackled the world of living organisms. It is their explanations of how adaptation arises that separates these thinkers. A few of the most significant ideas:^[21]

• Empedocles did not believe that adaptation required a final cause (~ purpose), but "came about naturally, since such things survived". Aristotle, however, did believe in final causes.
• In natural theology, adaptation was interpreted as the work of a deity, even as evidence for the existence of God.^[22] William Paley believed that organisms were perfectly adapted to the lives they lead, an argument that shadowed Leibniz, who had argued that God had brought about the best of all possible worlds. Voltaire's Dr Pangloss^[23] is a parody of this optimistic idea, and Hume also argued against design.^[24] The Bridgewater Treatises are a product of natural theology, though some of the authors managed to present their work in a fairly neutral manner. The series was lampooned by Robert Knox, who held quasi-evolutionary views, as the Bilgewater Treatises. Darwin broke with the tradition by emphasising the flaws and limitations which occurred in the animal and plant worlds.^[25]

Lamarck

• Lamarck's is a proto-evolutionary theory of the inheritance of acquired traits, whose main purpose is to explain adaptations by natural means.^[26] He proposed a tendency for organisms to become more complex, moving up a ladder of progress, plus "the influence of circumstances", usually expressed as use and disuse. His evolutionary ideas, and those of Geoffroy, fail because they cannot be reconciled with heredity. This was known even before Mendel by medical men interested in human races (Wells, Lawrence), and especially by Weismann.

Many other students of natural history, such as Buffon, accepted adaptation, and some also accepted evolution, without voicing their opinions as to the mechanism. This illustrates the real merit of Darwin and Wallace, and secondary figures such as Bates, for putting forward a mechanism whose significance had only been glimpsed previously. A century later, experimental field studies and breeding experiments by such as Ford and Dobzhansky produced evidence that natural selection was not only the 'engine' behind adaptation, but was a much stronger force than had previously been thought.^[27][28][29]

Types of adaptation

Adaptation is the heart and soul of evolution. Niles Eldredge^[30]

Changes in habitat

Before Darwin, adaptation was seen as a fixed relationship between an organism and its habitat. It was not appreciated that as the climate changed, so did the habitat; and as the habitat changed, so did the biota. Also, habitats are subject to changes in their biota: for example, invasions of species from other areas. The relative numbers of species in a given habitat are always changing. Change is the rule, though much depends on the speed and degree of the change.

When the habitat changes, three main things may happen to a resident population: habitat tracking, genetic change or extinction. In fact, all three things may occur in sequence. Of these three effects, only genetic change brings about adaptation.

Habitat tracking

When a habitat changes, the most common thing to happen is that the resident population moves to another locale which suits it; this is the typical response of flying insects or oceanic organisms, who have wide (though not unlimited) opportunity for movement.^[31] This common response is called habitat tracking. It is one explanation put forward for the periods of apparent stasis in the fossil record (the punctuated equilibrium thesis).^[32]

Genetic change

Genetic change is what occurs in a population when natural selection acts on the genetic variability of the population; moreover, some mutations may create genetic variation that will lead to differing characteristics of offspring and hence abet adaptation.^[33] The first pathways of enzyme-based metabolism may have been parts of purine nucleotide metabolism, with previous metabolic pathways being part of the ancient RNA world. By this means, the population adapts genetically to its circumstances.^[34] Genetic changes may result in visible structures, or may adjust physiological activity in a way that suits the changed habitat.

It is now clear that habitats and biota do frequently change. Therefore, it follows that the process of adaptation is never finally complete.^[35] Over time, it may happen that the environment changes little, and the species comes to fit its surroundings better and better. On the other hand, it may happen that changes in the environment occur relatively rapidly, and then the species becomes less and less well adapted. Seen like this, adaptation is a genetic tracking process, which goes on all the time to some extent, but especially when the population cannot or does not move to another, less hostile area. Also, to a greater or lesser extent, the process affects every species in a particular ecosystem.^[36][37]

Van Valen thought that even in a stable environment, competing species had to constantly adapt to maintain their relative standing. This became known as the Red Queen hypothesis.

Intimate relationships: co-adaptations

Main article: Co-adaptation

In co-evolution, where the existence of one species is tightly over bound up with the life of another species, new or 'improved' adaptations which occur in one species are often followed by the appearance and spread of corresponding features in the other species. There are many examples of this; the idea emphasises that the life and death of living things is intimately connected, not just with the physical environment, but with the life of other species. These relationships are intrinsically dynamic, and may continue on a trajectory for millions of years, as has the relationship between flowering plants and insects (pollination).

Pollinator constancy: these honeybees selectively visit flowers from only one species, as can be seen by the colour of the pollen in their baskets:

• 
• 
• 

• Co-extinction
• Infection-resistance
• Mimicry
• Mutualism
• Parasite-host
• Pollination syndrome
• Predator-prey
• Symbiosis

The gut contents, wing structures, and mouthpart morphologies of fossilized beetles and flies suggest that they acted as early pollinators. The association between beetles and angiosperms during the early Cretaceous period led to parallel radiations of angiosperms and insects into the late Cretaceous. The evolution of nectaries in late Cretaceous flowers signals the beginning of the mutualism between hymenopterans and angiosperms.^[38]

Mimicry

Main article: Mimicry

A and B show real wasps; the rest are mimics: three hoverflies and one beetle.

Henry Walter Bates' work on Amazonian butterflies led him to develop the first scientific account of mimicry, especially the kind of mimicry which bears his name: Batesian mimicry.^[39] This is the mimicry by a palatable species of an unpalatable or noxious species. A common example seen in temperate gardens is the hover-fly, many of which – though bearing no sting – mimic the warning colouration of hymenoptera (wasps and bees). Such mimicry does not need to be perfect to improve the survival of the palatable species.^[40]

Bates, Wallace and Müller believed that Batesian and Müllerian mimicry provided evidence for the action of natural selection, a view which is now standard amongst biologists.^[41] All aspects of this situation can be, and have been, the subject of research.^[42] Field and experimental work on these ideas continues to this day; the topic connects strongly to speciation, genetics and development.^[43]

• More on mimicry: Warning Colour and Mimicry Lecture outline from University College London

The basic machinery: internal adaptations

There are some important adaptations to do with the overall coordination of the systems in the body. Such adaptations may have significant consequences. Examples, in vertebrates, would be temperature regulation, or improvements in brain function, or an effective immune system. An example in plants would be the development of the reproductive system in flowering plants.^[44] Such adaptations may make the clade (monophyletic group) more viable in a wide range of habitats. The acquisition of such major adaptations has often served as the spark for adaptive radiation, and huge success over long periods of time for a whole group of animals or plants.

Compromise and conflict between adaptations

It is a profound truth that Nature does not know best; that genetical evolution... is a story of waste, makeshift, compromise and blunder. Peter Medawar.^[45]

All adaptations have a downside: horse legs are great for running on grass, but they can't scratch their backs; mammals' hair helps temperature, but offers a niche for ectoparasites; the only flying penguins do is under water. Adaptations serving different functions may be mutually destructive. Compromise and make-shift occur widely, not perfection. Selection pressures pull in different directions, and the adaptation that results is some kind of compromise.^[46]

Since the phenotype as a whole is the target of selection, it is impossible to improve simultaneously all aspects of the phenotype to the same degree. Ernst Mayr.^[47]

Consider the antlers of the Irish elk, (often supposed to be far too large; in deer antler size has an allometric relationship to body size). Obviously antlers serve positively for defence against predators, and to score victories in the annual rut. But they are costly in terms of resource. Their size during the last glacial period presumably depended on the relative gain and loss of reproductive capacity in the population of elks during that time.^[48] Another example: camouflage to avoid detection is destroyed when vivid colors are displayed at mating time. Here the risk to life is counterbalanced by the necessity for reproduction.

An Indian Peacock's train
in full display

The peacock's ornamental train (grown anew in time for each mating season) is a famous adaptation. It must reduce his maneuverability and flight, and is hugely conspicuous; also, its growth costs food resources. Darwin's explanation of its advantage was in terms of sexual selection: "it depends on the advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction".^[49] The kind of sexual selection represented by the peacock is called 'mate choice', with an implication that the process selects the more fit over the less fit, and so has survival value.^[50] The recognition of sexual selection was for a long time in abeyance, but has been rehabilitated.^[51] In practice, the blue peafowl Pavo cristatus is a pretty successful species, with a big natural range in India, so the overall outcome of their mating system is quite viable.

The conflict between the size of the human foetal brain at birth, (which cannot be larger than about 400ccs, else it will not get through the mother's pelvis) and the size needed for an adult brain (about 1400ccs), means the brain of a newborn child is quite immature. The most vital things in human life (locomotion, speech) just have to wait while the brain grows and matures. That is the result of the birth compromise. Much of the problem comes from our upright bipedal stance, without which our pelvis could be shaped more suitably for birth. Neanderthals had a similar problem.^[52][53][54]

Shifts in function

Adaptation and function are two aspects of one problem. Julian Huxley^[55]

Pre-adaptations

This occurs when a species or population has characteristics which (by chance) are suited for conditions which have not yet arisen. For example, the polyploid rice-grass Spartina townsendii is better adapted than either of its parent species to their own habitat of saline marsh and mud-flats.^[56] White Leghorn fowl are markedly more resistant to vitamin B deficiency than other breeds.^[57] On a plentiful diet there is no difference, but on a restricted diet this preadaptation could be decisive.

Pre-adaptation may occur because a natural population carries a huge quantity of genetic variability.^[58] In diploid eukaryotes, this is a consequence of the system of sexual reproduction, where mutant alleles get partially shielded, for example, by the selective advantage of heterozygotes. Micro-organisms, with their huge populations, also carry a great deal of genetic variability.

The first experimental evidence of the pre-adaptive nature of genetic variants in micro-organisms was provided by Salvador Luria and Max Delbrück who developed fluctuation analysis, a method to show the random fluctuation of pre-existing genetic changes that conferred resistance to phage in the bacterium Escherichia coli.

Co-option of existing traits: exaptation

Main article: Exaptation

The classic example is the ear ossicles of mammals, which we know from palaeontological and embrological studies originated in the upper and lower jaws and the hyoid of their Synapsid ancestors, and further back still were part of the gill arches of early fish.^[59][60] We owe this esoteric knowledge to the comparative anatomists, who, a century ago, were at the cutting edge of evolutionary studies.^[61] The word exaptation was coined to cover these shifts in function, which are surprisingly common in evolutionary history.^[62] The origin of wings from feathers that were originally used for temperature regulation is a more recent discovery (see feathered dinosaurs).

Related issues

Non-adaptive traits

Some traits do not appear to be adaptive, that is, they appear to have a neutral or even deleterious effect on fitness in the current environment. Because genes have pleiotropic effects, not all traits may be functional (i.e. spandrels). Alternatively, a trait may have been adaptive at some point in an organism's evolutionary history, but a change in habitats caused what used to be an adaptation to become unnecessary or even a hindrance (maladaptations). Such adaptations are termed vestigial.

Vestigial organs

Main article: Vestigiality

Many organisms have vestigial organs, which are the remnants of fully functional structures in their ancestors. As a result of changes in lifestyle the organs became redundant, and are either not functional or reduced in functionality. With the loss of function goes the loss of positive selection, and the subsequent accumulation of deleterious mutations. Since any structure represents some kind of cost to the general economy of the body, an advantage may accrue from their elimination once they are not functional. Examples: wisdom teeth in humans; the loss of pigment and functional eyes in cave fauna; the loss of structure in endoparasites.^[63]

Fitness landscapes

Main article: Fitness landscape

Sewall Wright proposed that populations occupy adaptive peaks on a fitness landscape. In order to evolve to another, higher peak, a population would first have to pass through a valley of maladaptive intermediate stages.^[64] A given population might be "trapped" on a peak that is not optimally adapted.

Extinction

Main article: Extinction

If a population cannot move or change sufficiently to preserve its long-term viability, then obviously, it will become extinct, at least in that locale. The species may or may not survive in other locales. Species extinction occurs when the death rate over the entire species (population, gene pool ...) exceeds the birth rate for a long enough period for the species to disappear. It was an observation of Van Valen that groups of species tend to have a characteristic and fairly regular rate of extinction.^[65]

Co-extinction

Main article: Co-extinction

Just as we have co-adaptation, there is also co-extinction. Co-extinction refers to the loss of a species due to the extinction of another; for example, the extinction of parasitic insects following the loss of their hosts. Co-extinction can also occur when a flowering plant loses its pollinator, or through the disruption of a food chain.^[66] "Species co-extinction is a manifestation of the interconnectedness of organisms in complex ecosystems ... While co-extinction may not be the most important cause of species extinctions, it is certainly an insidious one".^[67]

Flexibility, acclimatization, learning

Flexibility deals with the relative capacity of an organism to maintain themselves in different habitats: their degree of specialization. Acclimatization is a term used for automatic physiological adjustments during life; learning is the term used for improvement in behavioral performance during life. In biology these terms are preferred, not adaptation, for changes during life which improve the performance of individuals. These adjustments are not inherited genetically by the next generation.

Adaptation, on the other hand, occurs over many generations; it is a gradual process caused by natural selection which changes the genetic make-up of a population so the collective performs better in its niche.

Flexibility

Populations differ in their phenotypic plasticity, which is the ability of an organism with a given genotype to change its phenotype in response to changes in its habitat, or to move to a different habitat.^[68][69]

To a greater or lesser extent, all living things can adjust to circumstances. The degree of flexibility is inherited, and varies to some extent between individuals. A highly specialized animal or plant lives only in a well-defined habitat, eats a specific type of food, and cannot survive if its needs are not met. Many herbivores are like this; extreme examples are koalas which depend on eucalyptus, and pandas which require bamboo. A generalist, on the other hand, eats a range of food, and can survive in many different conditions. Examples are humans, rats, crabs and many carnivores. The tendency to behave in a specialized or exploratory manner is inherited – it is an adaptation.

Rather different is developmental flexibility: "An animal or plant is developmentally flexible if when it is raised or transferred to new conditions it develops so that it is better fitted to survive in the new circumstances".^[70] Once again, there are huge differences between species, and the capacities to be flexible are inherited.

Acclimatization

Main article: Acclimatization

If humans move to a higher altitude, respiration and physical exertion become a problem, but after spending time in high altitude conditions they acclimatize to the pressure by increasing production of red blood corpuscles. The ability to acclimatize is an adaptation, but not the acclimatization itself. Fecundity goes down, but deaths from some tropical diseases also goes down.

Over a longer period of time, some people will reproduce better at these high altitudes than others. They will contribute more heavily to later generations. Gradually the whole population becomes adapted to the new conditions. This we know takes place, because the performance of long-term communities at higher altitude is significantly better than the performance of new arrivals, even when the new arrivals have had time to make physiological adjustments.^[71]

Some kinds of acclimatization happen so rapidly that they are better called reflexes. The rapid colour changes in some flatfish, cephalopods, chameleons are examples.^[72]

Learning

Social learning is supreme for humans, and is possible for quite a few mammals and birds: of course, that does not involve genetic transmission except to the extent that the capacities are inherited. Similarly, the capacity to learn is an inherited adaptation, but not what is learnt; the capacity for human speech is inherited, but not the details of language.

Function and teleonomy

Adaptation raises some issues concerning how biologists use key terms such as function.

Function

To say something has a function is to say something about what it does for the organism, obviously. It also says something about its history: how it has come about. A heart pumps blood: that is its function. It also emits sound, which is just an ancillary side-effect. That is not its function. The heart has a history (which may be well or poorly understood), and that history is about how natural selection formed and maintained the heart as a pump. Every aspect of an organism that has a function has a history. Now, an adaptation must have a functional history: therefore we expect it must have undergone selection caused by relative survival in its habitat. It would be quite wrong to use the word adaptation about a trait which arose as a by-product.^[73][74]

It is widely regarded as unprofessional for a biologist to say something like "A wing is for flying", although that is their normal function. A biologist would be conscious that sometime in the remote past feathers on a small dinosaur had the function of retaining heat, and that later many wings were not used for flying (e.g. penguins, ostriches). So, the biologist would rather say that the wings on a bird or an insect usually had the function of aiding flight. That would carry the connotation of being an adaptation with a history of evolution by natural selection.

Teleonomy

Main article: Teleonomy

Teleonomy is a term invented to describe the study of goal-directed functions which are not guided by the conscious forethought of man or any supernatural entity. It is contrasted with Aristotle's teleology, which has connotations of intention, purpose and foresight. Evolution is teleonomic; adaptation hoards hindsight rather than foresight. The following is a definition for its use in biology:

Teleonomy: The hypothesis that adaptations arise without the existence of a prior purpose, but by the action of natural selection on genetic variability.^[75]

The term may have been suggested by Colin Pittendrigh in 1958;^[76] it grew out of cybernetics and self-organising systems. Ernst Mayr, George C. Williams and Jacques Monod picked up the term and used it in evolutionary biology.^{[77][78][79][80]}

Philosophers of science have also commented on the term. Ernest Nagel analysed the concept of goal-directedness in biology;^[81] and David Hull commented on the use of teleology and teleonomy by biologists:

Haldane can be found remarking, "Teleology is like a mistress to a biologist: he cannot live without her but he’s unwilling to be seen with her in public". Today the mistress has become a lawfully wedded wife. Biologists no longer feel obligated to apologize for their use of teleological language; they flaunt it. The only concession which they make to its disreputable past is to rename it ‘teleonomy’.^[82]

See also

Evolutionary biology portal

• Adaptive radiation
• Co-adaptation
• Co-evolution
• Ecological trap
• Evolvability
• Exaptation
• Intragenomic conflict
• Mimicry
• Polymorphism (biology)

References

1. ^ Huxley, Julian 1942. Evolution the modern synthesis. Allen & Unwin, London. p449
2. ^ Mayr, Ernst (1982). The growth of biological thought: diversity, evolution, and inheritance (1st ed.). Cambridge, Mass: Belknap Press. p. 483. ISBN 0-674-36445-7. "Adaptation... could no longer be considered a static condition, a product of a creative past, and became instead a continuing dynamic process." 
3. ^ Price P.W. 1980. The evolutionary biology of parasites. Princeton.
4. ^ The Oxford Dictionary of Science defines adaptation as "Any change in the structure or functioning of an organism that makes it better suited to its environment".
5. ^ Bowler, P.J. (2003) [1984]. Evolution: the history of an idea (3rd ed.). University of California Press. p. 10. ISBN 0-520-23693-9. 
6. ^ Patterson C. 1999. Evolution. Natural History Museum, London. p1
7. ^ Williams, George C (1966). Adaptation and natural selection: a critique of some current evolutionary thought. Princeton University Press. p. 5. ISBN 0-691-02357-3. http://books.google.com/books?id=p_UrcAAACAAJ. "Evolutionary adaptation is a phenomenon of pervasive importance in biology" 
8. ^ Mayr, Ernst (1963). Animal species and evolution (1st ed.). Cambridge: Belknap Press of Harvard University Press. ISBN 0-674-03750-2. 
9. ^ Mayr, Ernst (1982). The growth of biological thought: diversity, evolution, and inheritance (1st ed.). Cambridge, Mass: Belknap Press. pp. 562–566. ISBN 0-674-36445-7. 
10. ^ Salzburger W., Mack T., Verheyen E., Meyer A. (2005). "Out of Tanganyika: Genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes" (PDF). BMC Evolutionary Biology 5 (17): 17. doi:10.1186/1471-2148-5-17. PMC 554777. PMID 15723698. http://www.biomedcentral.com/content/pdf/1471-2148-5-17.pdf. 
11. ^ Kornfield, Irv; Smith, Peter (November 2000). "African Cichlid Fishes: Model Systems for Evolutionary Biology". Annual Review of Ecology and Systematics 31: 163. doi:10.1146/annurev.ecolsys.31.1.163. http://arjournals.annualreviews.org/doi/abs/10.1146/annurev.ecolsys.31.1.163. 
12. ^ Stebbins, G. Ledyard, Jr. 1950. Variation and evolution in plants. Columbia. Polyploidy, chapters 8 and 9.
13. ^ Margulis, Lynn (ed) 1991. Symbiosis as a source of evolutionary innovation: speciation and morphogenesis MIT. ISBN 0-262-13269-9
14. ^ Hutchinson, G. Evelyn (1965). The ecological theatre and the evolutionary play. Yale. ISBN 0-300-00586-5.  The niche is the central concept in evolutionary ecology; see especially part II The niche: an abstractly inhabited hypervolume. p26–78
15. ^ ^{a b} Dobzhansky, T.; Hecht, MK; Steere, WC (1968). "On some fundamental concepts of evolutionary biology". Evolutionary biology volume 2 (1st ed.). New York: Appleton-Century-Crofts. pp. 1–34. 
16. ^ Dobzhansky, T. (1970). Genetics of the evolutionary process. N.Y.: Columbia. pp. 4–6, 79–82, 84–87. ISBN 0-231-02837-7. 
17. ^ Dobzhansky T. (1956). "Genetics of natural populations XXV. Genetic changes in populations of Drosophila pseudoobscura and Drosphila persimilis in some locations in California". Evolution 10 (1): 82–92. doi:10.2307/2406099. JSTOR 2406099. 
18. ^ ^{a b} Endler, John A (1986). "Fitness and adaptation". Natural selection in the wild. Princeton University Press. pp. 33–51. ISBN 0-691-08387-8. http://books.google.com/books?id=MYk1XbelDssC&lpg=PA27&pg=PA33#v=onepage&q&f=false. 
19. ^ Sober, Elliott (1984). The nature of selection: evolutionary theory in philosophical focus. Cambridge, Mass: MIT Press. ISBN 0-262-19232-2. 
20. ^ Futuyma D.J. 1986. Evolution. 2nd ed, Sinauer, Sunderland, Massachusetts.
21. ^ references and details in their articles
22. ^ Desmond, Adrian 1989. The politics of evolution. Chicago. p31/32, footnote 18.
23. ^ In Candide, ou l'optimisme.
24. ^ Sober, Elliott 1993. Philosophy of biology. Oxford. Chapter 2
25. ^ Darwin, Charles. 1872. The origin of species. 6th edition, p397: Rudimentary, atrophied and aborted organs.
26. ^ see, for example, the discussion in Bowler, Peter H. 2003. Evolution: the history of an idea. 3rd ed, California. p86–95, especially "Whatever the true nature of Lamark's theory, it was his mechanism of adaptation that caught the attention of later naturalists". (p90)
27. ^ Provine, William 1986. Sewall Wright and evolutionary biology. University of Chicago Press.
28. ^ Ford E.B. 1975. Ecological genetics, 4th ed. Chapman and Hall, London.
29. ^ Orr H. (2005). "The genetic theory of adaptation: a brief history". Nature Rev. Genetics 6 (2): 119–127. doi:10.1038/nrg1523. PMID 15716908. 
30. ^ Eldredge, Niles 1995. Reinventing Darwin: the great evolutionary debate. Wiley N.Y. p33
31. ^ Eldredge, Niles 1986. Time frames: the rethinking of Darwinian evolution and the theory of punctuated equilibria. p136, Of glaciers and beetles.
32. ^ Eldredge, Niles 1995. Reinventing Darwin: the great evolutionary debate. Wiley, N.Y. p64
33. ^ C.Michael Hogan. 2010. Mutation. ed. E.Monosson and C.J.Cleveland. Encyclopedia of Earth. National Council for Science and the Environment. Washington DC
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35. ^ Mayr, Ernst (1982). The growth of biological thought: diversity, evolution, and inheritance (1st ed.). Cambridge, Mass: Belknap Press. ISBN 0-674-36445-7.  p481 (and sequence) tells how Darwin's ideas on adaptation developed as he came to appreciate it as "a continuing dynamic process" (bottom p483).
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