Evolutionary Microbiology

What did Darwin say about microbes,and how did microbiology respond?Maureen A. O’Malley

Egenis (ESRC Centre for Genomics in Society), University of Exeter, Byrne House, St Germans Road, Exeter, EX4 4PJ, UK

Opinion

Although it is commonly assumed that Darwin hadnothing to say about microbes, he did in fact say quitea lot. He included microbes in his Beagle studies of thegeographical distribution of organisms and used micro-scopic organisms as explicit exemplars of how adap-tation did not imply increasing complexity. Darwin oftendiscussed microrganismal classification, origins andexperimentation in his correspondence. But despitehis interests in microbial phenomena, Darwin’s impacton microbiological thinking of the late nineteenth cen-tury was negligible. This limited response may be con-nected to today’s assumptions about Darwin’s neglectof microbes.

Darwin and microbial evolutionIt is standard for biologists and even historians to say‘Darwin had nothing to say about microbes’, but in fact hedid (Box 1). Darwin’s early studies were of the biodiversityand geographic distribution of organisms, and he explicitlyincluded microorganisms in his global inquiry into thestructure of variation. Once his evolutionary explanationof variation had been published, Darwin found himselfobliged to rebut criticisms of natural selection that werebased on the apparent fact that microscopic organismsexhibited no evolutionary change. Darwin argued in thethird edition of The Origin [1] that these life forms wereappropriately fitted to ‘simple’ environments, and for thatreason did not evolve into more complex organisms. Heused this argument against the idea of evolution as a storyof increasing complexity. As a corollary to this centralargument, Darwin denied the simplicity of infusoria andmonads (Box 1) andmade several remarks that the evolvedcomplexity of their organization was evidence againstLamarck’s model of evolution.

These microbiological aspects of Darwin’s research andwriting are obviously not peripheral to it, and yet are rarelydiscussed in connection to either the content of his work orits historical impact. In what follows, I will examineexactly what Darwin said about microorganisms andwhy, and then how that was received by the emergingmicrobiological community of the late nineteenth century.This reception is probably the key reason for the disasso-ciation of Darwin and microbes that has persisted intocontemporary biology and history of biology.

Corresponding author: O’Malley, M.A. (M.A.O’Malley@ex.ac.uk)

0966-842X/$ – see front matter � 2009 Published by Elsevier Ltd. doi:10.1016/j.tim.2009.05.009

Assuming Darwin’s indifference to microbes andmicrobiologyIt tends to be taken for granted in discussions of Darwinand the genesis of his theory of evolution that he wasignorant of or indifferent to microbes and microbial evol-ution (e.g. [2–4]). If this were the case, it would require anexplanation because at the time of publishing On theOrigin of Species, the natural history of microbes wasflourishing, and medical and industrial microbiology (in-cluding brewing) were producing evidence that mademicrobes causally important biological agents. Louis Pas-teur [5] had just begun to publish his influential papersdemonstrating the role of microorganics in fermentation,and these herald the beginning of his experimental effortsto debunk spontaneous generation.

The ‘medicalization’ of microbiology was not, of course,the origin of microbiological research. The microscopicinvestigation of life began with Robert Hooke in his famedMicrographia [6,7] and many of the early detailed obser-vations of what are now called protists and prokaryoteswere made by Hooke’s contemporary, Antony van Leeu-wenhoek [8,9]. Their work began a natural history andexperimental tradition ofmicrobiology that flourishedwiththe development of microscopic technology and increasingcuriosity about the biological capabilities and origins ofthese miniscule lifeforms. The experimental approachunderpinned tests of various formulations of the spon-taneous generation hypothesis, which waxed and wanedin support from the seventeenth to the nineteenth century[10]. The natural history approach flourished whereverthere were microscopes, and led to intensive attempts toclassify the plethora of microbial discoveries made in thenineteenth century (Figure 1). Darwin was both an audi-ence of and a contributor to the natural history and exper-imental approaches to microbiology.

The foremost microbiologists of the time correspondedwith Darwin (e.g., Ferdinand Cohn, Christian GottfriedEhrenberg; see Figure 2). He read their work (e.g., RobertKoch’s, Louis Pasteur’s), commented on it to others, andeven invited Cohn to visit him at Down House (see Letters3490, 7471, 879of, 9810, 10618, and 11310 in the DarwinOnline Correspondence Project, www.darwinproject.ac.uk). Although Darwin did not draw heavily on themicrobial world for observational data in his own work,he used his and others’ knowledge of microorganisms tosustain his arguments about natural selection. These turns

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Box 1. ‘Microbes’ in the nineteenth century

The word ‘microbe’ was proposed by Charles Sedillot in 1878, and

subsequently popularized by Pasteur [50]. Microbe, and its counter-

part, ‘macrobe’ or macroorganism, are not used as biologically

coherent or evolutionarily meaningful terms. The aim of these terms

is simply to contrast the differences between multi-celled and single-

celled organisms. Microbes are negatively defined by being invisible

to the naked eye and by lacking multicellular complexity; macrobes

by a positive account of those features. In contemporary usage,

microbes include bacteria, archaea, protists and viruses. In Darwin’s

time, terms for microscopic organisms were in considerable flux. By

the 1870s, germ, bacterium, microbe, Protista, Monera, Protozoa and

fission-fungi were all used to describe sub-categories of microscopic

life [4,51] (Figure 1).

Darwin used a number of labels for microscopic lifeforms, not

always consistently or precisely: infusoria, secondary infusoria,

infusorial animalcules, protozoa, animalcules, monads and lower

organisms.

Infusoria is one of the older terms for microorganism, and was

coined by the German microscopist M. F. Ledermuller in 1763 [26]. In

Darwin’s writing and the common parlance of the time, infusoria

frequently referred to what are called protists today [52]. When

Darwin was speaking about the broader characteristics of microscopic

life, he would use infusoria, secondary infusoria or ‘infusoria and

other low organisms’ in this general sense. But in 1872, in the sixth

edition of The Origin, the first to contain a glossary (compiled by W.S.

Dallas), Darwin defined infusoria more restrictively as was becoming

common with the advent of tighter classification schemes [52]:‘IN-

FUSORIA. — A class of microscopic Animalcules, so called from their

having originally been observed in infusions of vegetable matters.

They consist of a gelatinous material enclosed in a delicate

membrane, the whole or part of which is furnished with short

vibrating hairs (called cilia), by means of which the animalcules swim

through the water or convey the minute particles of their food to the

orifice of the mouth.’ [53]

This use of Infusoria placed it within the Protozoa, which Darwin

also defined in his glossary:‘PROTOZOA. — The lowest great division

of the Animal Kingdom. These animals are composed of a gelatinous

material, and show scarcely any trace of distinct organs. The

Infusoria, Foraminifera, and Sponges, with some other forms, belong

to this division.’ [53]

Animalcule, Leeuwenhoek’s term for microorganism, is a consis-

tently more inclusive term, though Darwin uses it somewhat less than

infusoria:‘ANIMALCULE. — A minute animal: generally applied to

those visible only by the microscope.’ [53]

Monad is used to convey the notion of a fundamental self-

organized unit of life. Darwin sometimes refers to ‘primordial

monads’ as ancestral to all life [23 (p. 210)]. Although this use

equates monads with bacteria, Darwin tended to apply the term to

any unicellular lifeform.

Lower organism covers all non-multicellular life as well as ‘simple’

organisms such as sponges and nematodes. It is a commonly used

term in Darwin’s texts and those of his contemporaries.

Box 2. Microbe sampling on H.M.S. Beagle

‘Generally the atmosphere is hazy; and this is caused by the falling

of impalpably fine dust . . . I collected a little packet of this brown-

coloured fine dust... Professor Ehrenberg finds that this dust

consists in great part of infusoria with siliceous shields, and of the

siliceous tissue of plants. In five little packets which I sent him, he

has ascertained no less than sixty-seven different organic forms!

The infusoria, with the exception of two marine species, are all

inhabitants of fresh-water. . . . It is, however, a very singular fact,

that, although Professor Ehrenberg knows many species of infusoria

peculiar to Africa, he finds none of these in the dust which I sent

him. On the other hand, he finds in it two species which hitherto he

knows as living only in South America. . . . After this fact one need

not be surprised at the diffusion of the far lighter and smaller

sporules of cryptogamic plants’ [15,54].

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to microbiology evinced three main themes: (1) biogeogra-phical patterns and processes, (2) the distinction betweenevolution through natural selection and evolution as pro-gressive complexification, and (3) the continuous nature ofevolution operating on all lifeforms throughout the entirehistory of life.

Microbial biogeography

Darwin considered the biogeography of microbial life to bevery similar to that of macroorganisms, and biogeographyin general had formed his insights into evolution [11,12].His travels on H.M.S. Beagle and scrutiny of other collec-tions gave Darwin insight into the discontinuous distri-bution of different lifeforms, and a concomitant need toexplain such patterns. Natural selection eventuallybecame the ultimate explanation of the biogeographicdistribution of different lifeforms. Darwin involved Chris-tian Gottfried Ehrenberg (1795-1876), a highly reputedcollector and classifier of microscopic and botanical life(Figure 2), in his quest to understand microbial biogeogra-phy. He asked Ehrenberg, whom he described (perhaps forstrategic reasons) as ‘a great naturalist’ [13], to identify thewind-borne microbes that had covered the Beagle’s deck inthe form of dust. Darwin collected and sent these micro-organisms – specifically ‘infusoria’ (Box 1) – and othersamples (e.g., from the body paint of the Tierra del Fue-gians) to Ehrenberg for classification. Between 1844 and1846 they corresponded back and forth about possibledistribution patterns of the sampled infusoria (Box 2;see Letters 837, 747, 760, 845, 960 at www.darwinprojec-t.ac.uk) [14–17].

The distribution of microbial diversity was used byDarwin as evidence for his argument about dispersability(the capacity of organisms to disperse or be dispersed),which he saw as central to the geographical distribution ofspecies [18]. He preferred dispersal explanations to those

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involving geological disruptions, such as the loss of land-bridges proposed by Charles Lyell and Joseph Hooker[11,19]). Darwin made experiments on the viability ofseeds soaked in seawater [20], as well as numerous obser-vations and inferences about the dispersal mechanisms ofplants and animals, then successfully worked them into hisencompassing explanation of natural selection [12].Microbes and their distribution were just as explicitlyencompassed by this explanation.

The evolution by natural selection of microbes

Little was known about microbial physiology in the yearsin which Darwin developed his theory of natural selection.Taxonomies of microbes existed, however, and these beganto grow more systematically with the advent of FerdinandCohn’s classification scheme [21,22]. Darwin was wellaware of these developments. Nevertheless, it was lesspressing to explain largely invisible and always confusingmicrobial diversity than it was to make sense of the prolificnew discoveries of obvious diversity in the plant, animaland fungi world. These visible entities formed the primary

Figure 1. Images of microbes at the turn of the nineteenth and twentieth centuries.

Clockwise from top left: Bacillus anthracis with blood corpuscles (after Koch; from ‘Bacteriology’, in Encyclopaedia Britannica, 1911); various forms of bacteria with ‘cilia’

(ibid.); Phaeodaria (Plate 1 in Ernst Haeckel’s Kunstformen der Natur, 1904); Ciliata (Plate 3, ibid.); and Infusoria (Plate 23 in J.W. Griffith and A. Henfrey’s Micrographic

Dictionary, 3rd edition, 1875).

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evidential basis for Darwin’s theory of natural selection.Darwin, however, intended his theory of natural selectionto cover all life.

In 1861, responding to criticisms that the simplicity ofmicroscopic organisms disproved his theory of naturalselection (Box 3), Darwin added an argument about theadaptiveness of microbial organization to the third editionof The Origin [1]. Darwin’s statements on this subject camea few pages after the single diagram in The Origin, that ofthe tree of evolutionary speciation, and are part of arefutation of Lamarck’s ideas of the spontaneous gener-ation of simple life-forms that make evolutionary progressinto complex ones:

‘Why have not the more highly developed formseverywhere supplanted and exterminated the lower?Lamarck, who believed in an innate and inevitabletendency towards perfection in all organic beings,seems to have felt this difficulty so strongly, thathe was led to suppose that new and simple formswere continually being produced by spontaneousgeneration. I need hardly say that Science in herpresent state does not countenance the belief thatliving creatures are now ever produced from inor-ganic matter. If it were no advantage, these forms

would be left by natural selection unimproved or butlittle improved; and might remain for indefinite agesin their present little advanced condition. Andgeology tells us that some of the lowest forms, asthe infusoria and rhizopods, have remained for anenormous period in nearly their present state’ [1].

Darwin had written even earlier along these lines to hisfriend, geologist Charles Lyell (1797-1875), as they dis-cussed Lamarck’s ideas of evolution just prior to the pub-lication of the first edition of The Origin (Lyell had read aproof copy):

‘On the continuedCreation ofMonads.—This doctrineis superfluous (and groundless) on the theory ofNatural Selection, which implies no necessarytendency to progression. A monad, if no deviationin its structure profitable to it under its excessivelysimple conditions of life occurred, might remain unal-tered from long before the Silurian Age to the presentday. I grant there will generally be a tendency toadvance in complexity of organisation, though inbeings fitted for very simple conditions it would beslight and slow. How could a complex organisationprofit amonad? If it did not profit it there would be noadvance. The Secondary Infusoria differ but little

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Figure 2. Darwin surrounded by key nineteenth-century microbiologists.

Centre: Charles Darwin. Clockwise (from top left): Christian Gottfried Ehrenberg, Ferdinand Julius Cohn, Robert Koch and Louis Pasteur.

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from the living. The parent monad form might per-fectly well survive unaltered and fitted for its simpleconditions, whilst the offspring of this very monadmight become fitted for more complex conditions’ [23](p. 210)].

Darwin repeated this argument in many subsequenteditions of The Origin as well as in The Variation ofAnimals and Plants Under Domestication [24] (p. 8)] andshorter articles (see Box 4). He also discussed asexualreproduction, which he argued was not qualitatively differ-ent from sexual reproduction because both processes were‘determined by the same general causes’ and ‘governed bythe same laws’ [24 (p. 360)]. Sexual reproduction, however,could lead to greater stability of adaptation, although hedid not believe this advantage would account for the evol-ution of sex [24 (p. 362)]. In all these passages he isexplaining away any apparent trend to complexity acrossthe history of life and specific lineages. An evolvedtendency to inhabit ‘complex’ or highly variable environ-ments appears as complexification over time, but it isenvironmentally determined rather than determined byan innate evolutionary drive, and reversible if environ-mental conditions become ‘simpler’. Microbes were thecentral exemplars of this core point.

The continuity of evolved microbial complexity

Darwin argued that an evolutionary record could bedetected in the more simply organized life-forms, suchas monads, and also, that their minuteness must not blindthe natural historian to their organizational complexity(see Box 4). This perspective certainly had something to dowith the views of Ehrenberg, who was well known if notnotorious for having suggested that infusoria had systemsof organs – digestive, sexual, nervous – similar to those of

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animals. Darwin’s thoughts, however, were expressed withincreasing independence (especially as Ehrenberg rejectedthe theory of natural selection) [25,26],16]:

‘But to suppose thatmost of themanynowexisting lowforms have not in the least advanced since the firstdawnof lifewouldberash; for everynaturalistwhohasdissected some of the beings now ranked as very low inthe scale, must have been struck with their reallywondrous and beautiful organisation’ [27].

Darwin then used this complexity argument to specu-late on the continuous history of evolution and the commonancestor(s) of all living organisms:

‘The parent monad form [as the] one primordialprototype of all living and extinct creatures may, itis possible, be now alive!’ [23 (p. 210)].

In other words, Darwin saw in today’s monads a recordof the very earliest life-forms. Making this connectionbetween early and contemporary life, from monadsonwards, was an inevitable consequence of accepting des-cent with modification.

Summarizing Darwin’s views on the evolution ofmicrobesIn his discussions of themicrobial world, Darwin is makingat least three immensely important evolutionary claims.First, that all living entities, no matter how different theyseem from animals and plants, undergo natural selection,and second, that microbes demonstrate that evolution isnot a progression from simple to complex. The third argu-ment is that microbes and their adaptive capacities arevery important biological phenomena to understand if thehistory of evolution on Earth is to be understood. These

Box 3. Why stop at the limits of human vision?

Prior to the third edition of The Origin, Darwin had not explicitly

addressed the evolution of microbes in that text. One stimulus to do

so can be found in this review by J.A. Lowell in 1860.

‘Another serious objection to this theory is, that it may legitimately

be extended much farther than its author, unless it be in his final

summing up, has attempted. For why stop at the limits of human

vision? Why ignore the claims of the microscopic infusoria, hundreds

of which may nestle on the point of a needle? Nay, after the

microscope shall have reached its utmost perfection, there will be

myriads of created organisms, beyond its reach, to contend for the

honor of being the living representatives of our first ancestors.’ [55]

Box 4. Darwin’s views on adaptive simplicity

‘Animals may even become degraded, if their simplified structure

remains well fitted for their habits of life, as we see in certain

parasitic crustaceans. I have attempted to show (’Origin,’ 3rd edit. p.

135) that lowly-organized animals are best fitted for humble places

in the economy of nature; that an infusorial animalcule or an

intestinal worm, for instance, would not be benefited by acquiring a

highly complex structure. Therefore, it does not seem to me an

objection of any force that certain groups of animals, such as the

Foraminifera, have not advanced in organization. Why certain whole

classes, or certain numbers of a class, have advanced and others

have not, we cannot even conjecture. But as we do not know under

what forms or how life originated in this world, it would be rash to

assert that even such lowly endowed animals as the Foraminifera,

with their beautiful shells as figured by Dr. Carpenter, have not in

any degree advanced in organization.’ [27]

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themes are crucial to an understanding of the evolutionarytheory put forth by Darwin.

Today, despite the different evolutionary processesmany microbes are known to undergo (e.g., lateral genetransfer, speciation processes), Darwin’s basic principlesstill hold sway. What we see, therefore, in Darwin’s dis-cussions of microbes is the testing of a fundamental frame-work to see if it can accommodate all lifeforms and all oflife’s history. In this sense, Darwin’s investigations ofmicrobes gave his theory empirical support and the broad-est possible application. Could he have said more aboutmicrobes? Undoubtedly, but the strongest empirical evi-dence for evolution by natural selection came from moreestablished life sciences, the phenomena of which were notmediated by microscopic skill (a skill with which Darwinwas well acquainted). To establish his theory as solidly aspossible with the widest of audiences, Darwin focusedinstead upon the visible and the obvious.

The reception of Darwin’s evolutionary theory bymicrobiologistsDespite the above discussions of microbes in Darwin’s ownwords, they evoked muted reaction, whether from micro-biologists or other commentators. Microbiologists who didreflect on microbial evolution were not all of the sameopinion, however, and their responses to Darwin’s theoryof natural selection can be divided roughly into fourcategories: outright rejection, apparent endorsement, indif-ference and/or general scepticism, and medical application.

Outright rejection

This was a frequent response, in favour of other forms ofevolutionary theory, often because of the (misconceived)implications of Darwinian evolution, especially in relation

to spontaneous generation. Scientific advocacy of spon-taneous generation was in deep decline in the 1860s,due in large part to the perceived success of Pasteur’s‘falsifying’ experiments [28]. This was very much the casein Darwin’s milieu, and also in microbiological circles ingeneral. But many of these samemicrobiologists presumedspontaneous generation to be a logical component of evol-ution by natural selection, despite Darwin’s attempts toargue otherwise [1,23]. Ehrenberg, for example, stronglyopposed the notion of spontaneous generation, and this ledhim to reject evolution by natural selection because he didnot believe it could accommodate the development ofcapacities from monad to human [29] (p. 291), 16 (p. 7)].A similar stance can be found in the work of JamesSamuelson, a natural historian and microscopist whowrote broadly about biological matters. He carried outexperiments in the 1860s to demonstrate how a singlemonadic form developed into all the varieties of micro-scopic life from simple to increasingly complex. This devel-opmental theory, he argued to the Royal Society and toDarwin, removed the need for the ‘metaphysics’ of naturalselection and simultaneously refuted spontaneous gener-ation [30,31].Microbiology’s determination to eschew spon-taneous generation and all speculation about the origins oflife appears to have contributed to the formation of a deepgulf between the microbial world and the rest of life inregard to evolutionary theory. It would not be fully bridgeduntil the molecularization of microbiology in the twentiethcentury.

Apparent endorsement

The apparent endorsement of Darwin’s ideas sometimesinvolved the advocacy of a very different interpretation ofevolution than that proposed by Darwin. The famousDutch microbiologist and founder of the Delft School ofmicrobiology (retrospectively), Martinus Willem Beijer-inck (1851-1931) is a prime exemplar of such a response.Deeply impressed by Darwin, to the extent he prefaced hisdoctoral dissertation with a quote from The Variation ofPlants and Animals, Beijerinck nevertheless endorsed adevelopmental account of evolution, under which he sub-sumed Darwinian pangenesis, variability and heredity[32,33]. Also in this category we might place the greatmicrobial taxonomist, Ferdinand Cohn (Figure 2), who in1860 advocated Darwinian selection enthusiastically butprimarily in relation to the diversity and distribution of‘higher’ plants [34] (p. 50), 35]. By the 1880s, however, hehad become disenchanted with natural selection because itcould not explain the origins of life (and was thereforevulnerable to arguments about spontaneous generation)and possibly because he perceived Darwinian evolution tobe just too close to the transformism (the non-specificity ofspecies) against which he was battling [34 (p. 56)].

Indifference and/or general scepticism

This was a very common reaction to Darwinian evolution,due to the lack of understanding of microbial inheritance,and because of practical rather than theoretical concernswith variation. This category is probably where we findmost microbiologists of the late nineteenth century.Amongst them was Robert Koch (1843-1910; Figure 2),

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who as late as 1878 rejected the usefulness of a ‘magicwand of adaptation and inheritance’ to explain bacterialvariation [34 (p. 67)], preferring instead specific exper-imentation on the modification of laboratory-producedstrains [36]. An equally prominent figure in microbiology(despite being denigrated by Koch), was of course LouisPasteur (Figure 2), who was regarded with ‘infiniteadmiration’ by Darwin in 1863 [23 (p. 25)], but who neverreturned any similar compliment to Darwin [3,37]. In fact,the conservative arch-empiricist Pasteur mentioned Dar-win’s name just a single time, in 1876, when Pasteur notedwith relief that ‘transformism’ was finally waning, despitethe increasing appeal of Darwinism [38],37 (p. 409)]. Pas-teur’s politely coded reservations about Darwinian naturalselection are effectively captured in a short section of his1864 address to the Sorbonne:

‘Great problems are in question today, which keep allspirits in suspense: the unity or multiplicity ofhuman races; the creation of man several thousandyears or several thousand centuries ago; the fixity ofspecies or the slow progressive transformation of onespecies into another; the eternity of matter; the ideaof a useless God’ [39,40] (p. 344),3,41].

In the general context of French antipathy to the Eng-lish theory of evolution [42], there was a thin stream ofresearch that could have caused Pasteur to take morepositive notice of natural selection. This line of studyinvolved some very basic experimentation on the evolva-bility and adaptability of bacteria. William Dallinger(1839-1909), a cleric and a microscopist, carried out sevenyears of continuous culture experiments on three types ofmonad in order to examine each isolate’s capacity foradaptation to high temperatures. Through this researchhe hoped to ‘palpably demonstrate [Darwin’s] great doc-trine’ [43–46]. Darwin referred to these experiments as‘curious and valuable’, but never made more of them[47,46]. Pasteur, deeply committed to experimentationrather than historical inference [39], would probably havefound such experimentation a stimulus to think morethoroughly about Darwinian natural selection hadhe encountered Dallinger’s work. There is no indicationhe did either.

Medical application

Medicine was, curiously, where Darwinian evolutionarytheory did find a temporary footing, primarily in relation tothe concept of specificity and the tumultuous variation ofthe microbial world [41]. The problem of disease causationand its changeability needed explanation, and for somemedical microbiologists, Darwinian natural selection wasable to supply a better and more unifying account ofperplexing variability than anything else available. Vari-ation in disease agents could then be understood not asessentially random and lawless, but as ordered by selec-tion. High generation rates allowed more variation tomanifest and be selected as environmental conditionschanged, thus ruling out spontaneous generation of newagents of disease [41]. In the long run, however, theseefforts to incorporate Darwinian thinking into medicalpathology dwindled as heredity became a ‘fixed’ phenom-

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enon and the variable causes of infection were locatedwithin species, thereby removing the role of natural selec-tion in explaining alterations in virulence as speciation[48,49]. Exacerbating this decline in Darwinian medicinewas the general lack of microbiological attention to evol-ution, which resulted in the twentieth-century struggle tounite evolutionary biology with microbiology.

The historical basis for assuming Darwin said nothingabout microbesIt is clear that Darwin did consider the microbial world andthat he made important claims about microbial evolution.Why, then, is it standard to assume now that Darwinignored microorganisms? The most straightforward con-clusion to draw is that the response of the nineteenth-century microbiological community to Darwin’s theory ofevolution is largely responsible for contemporary assump-tions that Darwin never thought about and neverresearched microbes. Few nineteenth-century microbiolo-gists, whether of the natural history or experimental com-munities, found evolution by natural selection applicable tomicroorganismal research, especially when it appeared toallow spontaneous generation and to introduce too strong anotion of species change. Outright rejection of natural selec-tion could also be ignored if it were articulated by somebodysuch as Ehrenberg, whose star was on the wane because ofhis exaggerated and unsupported interpretations of thecomplexities of protist intracellular structure [29,26]. Con-sequently, when we look back now, we find that the bignineteenth-century debates over Darwin were primarilyabout the evolution of animals, especially Homo sapiens.Medical microbiology and epidemiology, having brieflyfound succour in Darwin, then proceeded at best to takeevolutionasageneralbackgroundconditionrather thanasatopic for further investigation in relation to health.

Microbes then and often now take on an aura ofinvisibility in the public arena. The rise of fields suchas metagenomics and the attention it draws to micro-biogeochemistry has created a highly favourable contextfor wider recognition of the importance and extent of themicrobial world, just in time for the 2009 ‘Darwin year’and its refocusing of attention on what he did say. By nomeans does this imply that Darwin’s general frameworkdoes not need supplementing by the very specific differ-ences in microbial evolution. However, despite all that isknown now, the basic framework of natural selection thatDarwin tested on microbes still stands.

AcknowledgementsMany thanks to Ford Doolittle for suggesting I do some research on thistopic, and to John Dupre, Sabina Leonelli, Staffan Muller-Wille, SteveHughes and Dan Nicholson for very helpful comments on an earlier draft.Pierre-Olivier Methot provided some crucial references on Darwin andmedicine in the nineteenth century. Two anonymous referees suggested anumber of important clarifications and elaborations, the paper structurewas suggested by the journal. Research for this article was funded by theESRC Genomics Network at Egenis, University of Exeter.

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