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Home , Francesco Redi, Helix (gastropod), Nicolaas Hartsoeker

Evolutionary Anthropology 13:5–10 (2004)

CROTCHETS & QUIDDITIES

The in Taffeta Pants

KENNETH WEISS

What is the magic that makes dead flesh fly? himself gave up on the preformation view). These various intuitions arise natu- Where does a new come from? manded explanation. There was no rally, if sometimes fancifully. The nat- Before there were , and compelling reason to think that what uralist Henry Bates observed that the before the theory, this was not a one needed to find was too small to natives in the village of Aveyros, up trivial question. Centuries of answers see. hypothesized epigenesis, the Tapajos tributary to the Amazon, were pure guesswork by today’s stan- a kind of of believed the fire ants, that plagued dards, but they had deep implications life from the required materials (pro- them horribly, sprang up from the for the understanding of life. The vided in the ), that systematic ob- blood of slaughtered victims of the re- 5 phrase spontaneous generation has servation suggested coalesced into a bellion of 1835–1836 in Brazil. In gone out of our vocabulary except as chick. Such notions persisted for cen- fact, Greek mythology is full of beings an historical relic, reflecting a total turies into what we will see was the spontaneously arising—snakes from success of two centuries of biological critical 17th century, when the follow- Medusa’s blood, Aphrodite from sea- research.1 The realization that a new ing alchemist’s recipe was offered for foam, and others. Even when the organism is always generated from the production of mice:3,4 mix sweaty truth is known, we can be similarly one or more cells shed by parents ex- underwear and wheat husks; store in impressed with the phenomena of plained how something could arise open-mouthed jar for 21 days; the generation. John Muir observed, “The where nothing could be seen. sweat will penetrate the wheat, chang- bluebottle is abundant in these Yo- However, if this solved one question ing it into mice. semite woods, ever ready with his about the origin of organisms, it left a There was an equally persistent al- marvelous store of to make all 6 related problem that is still with us, ternative view. In 50 BC, Lucretius (de dead flesh fly.” that of explaining autonomous gener- Rerum Natura) wrote that “The first ation—development—which has be- bodies of each thing must be inside TWO CENTURIES AT THE come a core question in modern biol- the seed; because of this all things can ogy and , and is relevant to the not arise from anything. For each par- OF physical and behavioral traits that are ticular seed has, in itself, hidden in- The scientific assault on the ques- at the heart of anthropology. Where side its own distinctive powers.” It tion began in earnest in the 17th cen- do they come from each generation? seemed reasonable to assume conti- tury,2,7 but took two centuries to com- nuity in nature, so that what we see plete. The most famous example of OMNE VIVUM EX VIVO? reflects what happens before we can spontaneous generation was the ap- see it, making it logical to infer that pearance of in dead meat. In The ancients knew about parents either the sperm or egg contained a 1668 Francesco Redi (Figure 2) per- producing offspring of their own kind, future organism in miniature, an is- formed a classic study8 that some con- but also that there isn’t a chicken in- sue long and hotly debated between sider to have been the first controlled side an egg when it is freshly laid.1,2 It the “ovist” and “spermist” schools of in the . was not just a lack of microscopes that thought. The imagery of preformation He put dead flesh in an open dish, in made this latter fact one that de- has been made famous by countless which maggots soon appeared as ex- reprinting of Nicolaas Hartsoeker’s pected. I never realized until I re- 1694 AD drawing (Figure 1). An impli- peated the for this column cation was that an organism’s gonads (Figure 3) that if you were not aware Ken Weiss is a biological anthropologist, contain, in ever more miniaturized of the tiny fly eggs, the maggots make at Penn State University. E-mail: kmw4@ and nested form, the preformed em- psu.edu their appearance, dramatically, bur- bryos of all its potential future descen- rowing out from the inside, the whole dants. Biblical scholars related this to piece of flesh subsequently throbbing © 2004 Wiley-Liss, Inc. a preordained course of human be- like a heart before being transformed DOI 10.1002/evan.30001 Published online in Wiley InterScience ings from Adam to Armageddon almost entirely into . No won- (www.interscience.wiley.com). (though after later work, Hartsoeker der the explanation that had been 6 Weiss CROTCHETS & QUIDDITIES

swarming around the gauze and lay- count their persistence in centuries,”4 ing eggs on it that quickly hatched as but that did not make them right. A maggots. Dead flesh does not fly of its fighter like Huxley, he was determined own accord. to prove the errors of rivals like the This was not entirely the end of a famous Comte de Buffon and his own story whose importance even to late peer Felix Pouchet, who advocated 19th century science was reflected in molecular vitalistic versions of epi- the famous 1870 Presidential address genesis. In experiments beginning in by Thomas Huxley (Figure 4) to the Darwin’s year, 1859, that essentially British Association for the Advance- refined Redi’s logic, Pasteur placed ment of Science.9 If Redi had shown fresh, boiled broth in a flask con- that complex like insects did structed with an S-shaped neck that not arise spontaneously, this did not kept from settling account for the appearance of tiny from the air onto the broth, and no “” when substances like fermentation occurred. With this beef broth, infusions of grain or hay, proof that microbes, too, arise only grapes, and many other things de- from parents of like type, Pasteur pro- cayed or fermented. These had been vided another instance of what Hux- observed since the early days of mi- ley called “the great tragedy of Sci- croscopy. Could this simple form of ence—the slaying of a beautiful life arise spontaneously? Attempts to hypothesis by an ugly fact.” Not even repeat Redi’s experiments in regard to tiny microbes arise by themselves. the origin of this primitive life-form I’m omitting many details of a long were notoriously inconsistent, ex- history,1,2,7 but Pasteur and Huxley plaining why the issue could remain were both clear about the importance for so long a central question in biol- of a proper understanding of micro- ogy. The problem (we now know) was bial generation. That had enormous the incomplete elimination of boiling- implications for agricultural pest con- resistant spores, cells too small to fil- trol and manufacturing (e.g., wine, ter by the means that were tried, and baking, beer, silk), and for public the ubiquity of microbial life in the air health. Huxley raised the additional around us. and unanswered question of xenogen- The fermentation question was fi- esis, the appearance of tumors nally put to rest by the vigorous ener- and plant galls: what form of new life Figure 1. Homunculus (Hartsoeker, 1694, Es- gies of another of the century’s great were these, that sprung up within an say de Dioptrique). science entrepreneurs, organism? (Figure 5), in promoting his microbial If even complex organisms come given! But if Redi covered an identical view of the world. In an 1864 address from other life, what is the contribu- container with fine gauze, no maggots to the Sorbonne Scientific Soire´e he tion of male and female and why are appeared. Instead, he observed flies noted that “the most striking errors both needed? Was the fly contained in

Figure 2. Pioneers (A) Francesco Redi. (B) Title page (5th ed., 1688). (C) . Portrait sources: Spallanzani www. chemheritage.org/EducationalServices/pharm/antibiot/activity/spapas.htm Redi: www.francescoredi.it/ CROTCHETS & QUIDDITIES The Frog in Taffeta Pants 7

Figure 3. Redi redux triptych (2003 AD). (A) desirous. (B) Fly eggs after 24 hours (arrows show a few). (C) Riddled with maggots and pulsating after 48 more hours (arrows show a few).

the egg, or sperm? We think of ovists tity needing only chemical stimula- teins and other compounds; 3) ligand- versus spermists as quaint naivety, tion by the seminal fluid.1,7 Actually, receptor binding involved in the but when microscopists demonstrated in the end Spallanzani concluded that receipt of extracellular signals that parthenogenesis in aphids, it seemed something in the thicker fraction of change gene expression within cells; an important issue. To address it, Laz- semen was responsible, because he 4) protein-DNA binding that allows zaro Spallanzani (Figure 2) per- could not accept that it was its wriggly transcription factor proteins to ex- formed a series of clever experiments contaminants. press or repress specific genes based in the 1760s. Semen was known from on regulatory sequences in DNA lo- to contain wormified be- THE MODERN VIEW: cated near the genes;13 and 5) the ings in a thicker component, and a AUTONOMOUS GENERATION sensing of extra-cellular conditions thinner liquid. Spallanzani dressed (such as pH or salt concentrations) to male in tight-fitting taffeta pants Hartsoeker’s homunculus and frogs which cells can actively adjust (e.g., and let them “seek the female with wearing taffeta condoms draw smiles, ion channels, neurotransmission). equal eagerness, and perform, as well because we are now completely con- It is not just its genome but the rel- as they can, the act of generation.”10 vinced not just that all life comes from ative timing and use of context-spe- other life, but of Virchow’s additional (cited in Moore1). All jokes about am- cific subsets of a ’ genes that dictum that all cells come from other orous frog Princes aside, the males’ produces all complex organisms. Fig- cells. But we should think a little more modest attire prevented the denser ure 6 is a schematic representation of carefully, because showing that a new fraction from reaching the eggs, and the way this works. S number repre- life only comes from other life forces this prevented fertilization: the egg sents signaling factors released by the question how it happens. The an- was not the ovist’s self-contained en- cells (not shown) and received by tar- swer is as remarkable as the notion of get-cell receptors indicated by arrows spontaneous generation could ever entering the latter, and G number in- have been, and ties together elements of preformation and epigensis as well. dicates specific genes expressed After all, what is a new human life? within each cell. The hierarchy of sig- A fertilized egg has no limbs, sense of naling switches leads to hierarchically humor, or hair. Yet, this single cell is differentiated combinatorial gene ex- in many ways an autonomous entity pression among the cells in an organ- that really does develop spontane- ism. Since the cells are otherwise se- ously from raw materials. In the mod- questered from each other, local ern view the key is DNA. The notion of tissues can develop independently— the genome as an information-storage autonomously. For this reason, local unit may be an overworked metaphor gene combinations that include some of our computer age,11,12 but fertilized overlapping genes can specify unre- eggs do, after all, turn into people. lated structures (e.g., G1 and G4 in the Perhaps even more profound is that figure).14,15–17 the same few basic processes trans- Internal conditions start a cell off by form raw materials into people and controlling the expression of an initial oak trees. These include 1) comple- set of genes. Those conditions are not mentary base-pairing of DNA and “spontaneous” in that they include pa- Figure 4. Thomas Huxley as President of the RNA (A with T, C with G); 2) the spec- rental mRNA as well as the right as- BAAS (from The Period, Nov 26, 1870). ificity of interactions between pro- semblage of and other 8 Weiss CROTCHETS & QUIDDITIES

components have built into them the legacy of 3ϩ billion years of prior an- cestry.

KICKING THE PRIMAL SOUP UP TO NOTCHES UNKNOWN The modern denial of spontaneous generation is not quite as total as it may seem, because we are merely de- ferring the question of the origin of life itself back to a sufficiently remote time when, in what Huxley called “an act of philosophical faith,” we can safely assume that spontaneous gen- Figure 5. Louis Pasteur. (A) Portrait. (B) S-shaped experimental flask. Pasteur: www. eration did occur. In fact, given that accessexcellence.org/AB/BC/Louis_Pasteur.html. assumption, it is not surprising that there are efforts to develop a recipe by which we, too, can create new life chemicals. But once this begins, cells The difference between you and an from scratch.18 produced by subsequent mitosis re- oak tree is due to DNA sequence dif- The goal is to synthesize a func- tain their expression profiles until sig- ferences. It is this “information” that tional organism, not just fire up self- naled to change. Thus, the genes that allows the cell to develop autono- sustaining biochemical reactions. set up the anterior-posterior body axis mously without instruction imposed Craig Venter, the Dark Force who lead to the expression of genes related from the outside and without the need challenged NIH to a race to sequence to the formation of vertebrae, but be- for an organism-in-miniature. This is the human genome, and several other cause the latter occurs later in the em- also why the system is universal from groups, are attempting to identify the bryo, the genes expressed in different microbe to macro-organism. minimal set of genes that would suf- parts of the vertebral column are dif- So, in meaningful ways, by starting fice. A combination of approaches is ferent, and so are the resulting verte- out life as a single cell you really were being taken, using simple single- brae. This is a temporally forward, preformed in your genome, and you celled organisms. The approaches in- conditional (context-specific) process really were generated by epigenesis clude comparing the gene sets of very of differential, combinatorial gene ex- out of non-living materials. But far distantly related , the system- pression that does not look backward, from spontaneous assembly out of un- atic experimental inactivation of either within the organism or from formed raw materials, and far from genes, one by one, to see which are the organism to its parents. Subsets of containing the preformed miniatures needed and which dispensable, and the tree of developmental descent are of all future generations, the genetic even the stepwise assembly of artifi- themselves as autonomous as the original egg was (thus, germs can be cultured and develop in vitro). It is this developmental unfolding (the original use and meaning of the term “”) of what is already there that makes a complex organism. DNA settled the ovist-spermist de- bate, and also accounts for xenogen- esis. Viruses and somatic mutation, unknown to Huxley, can cause tumors by introducing new or modified DNA into a cell. This directly affects the cell in which it occurs, not the whole or- ganism, but the affected cell can then proliferate, generating a new, partially autonomous tree of descent within, but not part of, the organism, one of the major killers of our time. We don’t consider a tumor to be a new kind of organism or species, but it is easy to see that it blurs the distinction be- tween notions of spontaneous genera- Figure 6. Schematic of hierarchical gene regulatory cascade by which hierarchically tion and parental transmission. autonomous development is controlled (see text). CROTCHETS & QUIDDITIES The Frog in Taffeta Pants 9

self-assemble into a cell with new membranes and then replicate—and do it without any pre-existing RNA (like the maternal mRNA that got each of us going). And all indications so far are that even after this neo- alchemy, we will have to supply a spark of existing life of some kind—to “shake well before using.” Even when this is done it will in no way be spontaneous generation of life congealing in an artificial NeoPrimal Soup. Life generated in vitro will be based on assembling pre-existing genes that we discover, and they will be genes with 3ϩ billion years’ evolu- tionary maturity. At best, a test-tube cellular baby might be viewed as spontaneous (and artificial) specia- tion. We already can engineer genes into existing species, like herbicide resis- tant genes in corn or soy beans. This and more extensive genetic engineer- ing will undoubtedly occur in the fore- seeable future. Such changes are the spontaneous introduction, not gener- ation, of new traits. They may have widespread effects on the organism, but even this would be neither the spontaneous generation of an organ- ism or even of a gene, because we would be simply modifying or trans- ferring an existing evolutionary prod- uct (the gene). However, we can dream. It is possi- Figure 7. “Evolution” Emerging: dead flesh flies with pupae waiting in the wing. ble to synthesize random sequences, and screen them in vitro to find ones that served some prespeci- cially synthesized known candidate survive in the loving care of a lab tech- fied function like resistance to micro- genes (polio virus has already been nician in a highly controlled environ- bial attack or speeding up some met- generated this way19) to see what is ment. It would not be an organism in abolic process, then back-translating the winner into corresponding DNA needed. Because the work is in the usual sense; what it takes to be a sequence and introducing the result- progress and may have commercial real minimal being and how the exist- ing gene into a species. That would be value, public details are hard to come ing ones got that way are subtle.22 a new, in a sense, spontaneous, prod- by, but results so far suggest that only Attempts like these are relevant to uct that will be highly touted as hav- a few hundreds of genes are the issue of spontaneous generation. ing got us much closer to Genesis. It is needed.20,21 These are involved in en- The Minimal Being will resemble nei- likely to happen, perhaps soon (phar- ergy metabolism, DNA replication, ther the first life nor any existing life. maceutical firms are working in direc- and protein translation. Making a When successfully created, it will not tions of this sort). But a gene is not an Minimal Being with these abilities be spontaneously or probably not organism, and it will be some time would demonstrate that some mini- even autonomously generated. The before we can synthesize those any- mal functional set of genes is viable. cell was evolution’s Great Leap For- where outside of Hollywood. But the achievement would be tem- ward from the biochemistry of Primal Truly spontaneous generation in pered by the fact that we already know Soup. But so far we know of no way nature would play havoc with evolu- these basic functions are needed and other than nature’s way to make the tionary biology, which is based en- have worked out their genetics. The membranes that are fundamental to tirely on the concept of all life having Minimal Being would be so crippled all cells. To mimic real life we need to diverged from essentially a single and of natural function that it could only set up a tubeful of chemicals that first ancient common origin. But if life 10 Weiss CROTCHETS & QUIDDITIES could arise all by itself once, why Tuana, and John Fleagle for critically 10 Spallanzani L. 1784. Dissertations relative to doesn’t spontaneous generation, at least reading this manuscript. the of animals and vegetables. London: Murray. of the primeval kind, still occur? Per- 11 Lewontin RC. 2000. The triple helix. Cam- haps it does. The raw ingredients are ERRATUM bridge, MA: Harvard University Press. everywhere. In fact a recent experiment 12 Kay L. 2000. Who wrote the book of life? showed that random short strings of A typo that neither Word nor I spot- Stanford, CA: Stanford University Press. ted in my installment “Dinner at Ba- 13 Weiss KM. 2002. Is the message the medium? amino acids could rather easily gener- Biological traits and their regulation. Evol An- ate fundamental biological proper- by’s” (Vol. 12, p. 247) compares brut- thropol 11:88–93. ties.23 But whether or not rudimentary ish brutes to “advanced and gentile” 14 Davidson EH. 2001. Genomic regulatory sys- biochemistry is taking place in the soil, humans. No compliment to any reli- tems: Development and evolution. San Diego, CA: Academic Press. sea, or air around us is basically irrele- gion was intended, as all are (hope- fully) “gentle.” 15 Gerhart J, Kirschner M. 1997. Cells, embryos, vant to evolutionary biology. and evolution: Toward a cellular and develop- Any such activity would be based on mental understanding of phenotypic variation and evolutionary adaptability. Malden, MA: primitive molecular interactions that REFERENCES Blackwell Scientific. cannot compete with organized life 16 Gilbert S. 2001. . 6 ed. (which would probably just eat it up Many things discussed here can be Sunderland, MA: Sinauer. at every encounter). There is no evi- profitably explored by web searching. 17 Carroll S, Grenier J, Weatherbee S. 2001. From DNA to diversity: Molecular genetics and dence whatever of brand new life 1 Moore JA. 1993. Science as a way of knowing: the evolution of animal design. Malden, MA: evolving clades of differentiation, au- The foundations of modern biology. Cambridge, Blackwell. MA: Harvard University Press. tonomy, or complexity. There is only 18 Ainsworth C. 2003. The facts of life. New Sci- 2 Pinto-Correia C. 1997. The ovary of eve: Egg entist 178:28–31. one of that kind of life, and the truly and sperm and preformation. Chicago: Univer- sity of Chicago Press. 19 Cello J, Paul AV, Wimmer E. 2002. Chemical spontaneous generation we assume synthesis of poliovirus cDNA: generation of in- once did occur was only of the sim- 3 van Helmont J-B. 1671. On the necessity of fectious virus in the absence of natural template. leavens in transformations. In: Conte JL, editor. Science 297:1016–1018. plest of biochemical processes, not Les oevres de Jean-Baptiste van Helmont. Lyon. bluebottle flies or fire ants. Today, 20 Mushegian AR, Koonin EV. 1996. A minimal 4 Pasteur L. 1864. On spontaneous generation. gene set for cellular life derived by comparison of only a fly can make dead flesh fly. This In: Levine A, Latour B, editors. Sorbonne Scien- complete bacterial genomes. Proc Natl Acad Sci was what Pasteur showed “with exper- tific Soiree; 1864; . U S A 93:10268–10273. 5 Bates HW. 1863. The naturalist on the River 21 Kobayashi K, Ehrlich SD, Albertini A, Amati iments so gripping that you cannot Amazon. London: J. Murray. 4 G, Andersen KK, Arnaud M, Asai K, Ashikaga S, fail to remember them.” 6 Muir J. 1911. My first summer in the Sierra. Aymerich S, Bessieres P, Boland F, Brignell SC, New York: Houghton Mifflin. Bron S, Bunai K, Chapuis J, Christiansen LC, 7 Hankins TL. 1985. Science and the Enlighten- Danchin A, Debarbouille M, et al. 2003. Essential NOTES ment. Cambridge, England: Cambridge Univer- bacillussubtilis genes. Proc Natl Acad SciUSA sity Press. 100:4678–4683. I welcome comments on this col- 8 Redi F. 1668. Esperienze intorno alla generazi- 22 Maniloff J. 1996. The minimal cell genome: umn: [email protected]. I maintain one degl’ insetti. : Stampiera de Piero “on being the right size.” Proc Natl Acad Sci Crotchety Comments on my web page: Matini. U S A 93:10004–10006. 9 Huxley TH. 1870. and . 23 Keefe AD, Szostak JW. 2001. Functional pro- www.anthro.psu.edu/rsrch/weiss lab. London: British Association for the Advance- teins from a random-sequence library. Nature htm. I thank Anne Buchanan, Nancy ment of Science. 410:715–718.

Articles in Forthcoming Issues

• The Oldest Ape Laura MacLatchy • Evolutionists and Creationists at the Dinner Table George Armelagos • New Views on Tree Shrews: The Role of Tupaiids in Primate Supraordinal Relationships Eric Sargis • Complementary Approaches of Cytogenetics and Molecular Biology to the and the Study of Speciation Processes in Lemurs Ives Rumpler • A Re-Evaluation of the Ecological, Behavioral and Anatomical Adaptations of the Goeldi’s Monkey: New Data and Their Implications for Understanding Callitrichine Evolution Leila Porter and Paul Garber