SPOTLIGHT

Inclusion and exclusion in the history of developmental biologyNick Hopwood

ABSTRACTScientific disciplines embody commitments to particular questionsand approaches scopes and audiences they exclude as well asinclude Developmental biology is no exception and it is useful toreflect on what it has kept in and left out since the field was foundedafter World War II To that end this article sketches a history of howdevelopmental biology has been different from the comparativehuman and even experimental embryologies that preceded it as wellas the embryology that was institutionalized in reproductive biologyand medicine around the same time Early developmental biologylargely excluded evolution and the environment but promisedto embrace the entire living world and the whole life courseDevelopmental biologists have been overcoming those exclusionsfor some years but might do more to deliver on the promises whilecultivating closer relations not least to reproductive studies

KEY WORDS British Society for Developmental Biology (BSDB)Comparative experimental and human embryology History ofembryology Reproductive biology and medicine Society forDevelopmental Biology (SDB)

IntroductionLast yearrsquos 70th anniversary of the British Society for DevelopmentalBiology (BSDB) was an opportunity to stand back to considerhow the subject came about and what has made it distinctive and toreflect on present arrangements This historical commentary takesstock through the theme of inclusion and exclusionScience is organized into disciplines that shape training identity

and funding they define the important problems and how theseshould be addressed Disciplines are made not found Making oneis a political project of carving out questions approaches and scopeand recruiting patrons and audiences in relation to what went beforeand to other sciences (eg Nyhart 1995 Lenoir 1997) Claiming anidentity involves deciding what to include or exclude what will bein and what will be out Practitioners negotiate the boundaries oftheir own field and the terms of their relations with neighboursDevelopmental biologists have done this explicitly in electing not tomerge with cell biology societies in the 1980s and early 1990s and inthe BSDBrsquos 2013 decision not to add lsquostem cellrsquo to its name [For apossible merger of the BSDBwith the British Society for Cell Biologysee Martin Johnsonrsquos Chairmanrsquos report 1985-86 BSDB Newsletterno 13 (Spring 1986) pp 10-11 (1986-1(13) at bsdborg20180429bsdb-archive) For the 1992 vote against merging the (American)Society for Developmental Biology and the American Society for CellBiology see SDB and ASCB records (libraryumbceduspeccollfindingaidscoll022php and libraryumbceduspeccollfindingaidscoll008php) For the stem cell vote see Martinez Arias (2013)]

In this view when lsquodevelopmental biologyrsquo was founded afterWorld War II it was not just another word for embryology (Horder2010) Nor has it been simply an expanded version althoughlsquoexperimental embryology across the living worldrsquo used to comeclose and the field has broadened in recent decades It is also astretch to present developmental biology as lsquothe stem cell ofbiological disciplinesrsquo (Gilbert 2017) That is because ndash to begincloser to the beginning ndash 18th-century lsquogenerationrsquowas the commonancestor of embryology as well as research on heredity andreproduction while anatomy gave rise to many other sciences(Jacob 1982 Hopwood 2018a Cunningham 2010) Nineteenth-and early 20th-century embryology did then contribute to severalfields including immunology and genetics yet developmentalbiology was not there from the start but was itself lsquobudded offrsquo It ismore accurate and more respectful of the differences to think interms of a family of disciplines or research programmes that haveshared interests in embryos and in development but had their ownidentities and asked somewhat different questions (Hopwood 2009)

I shall argue for the distinctiveness of developmental biology byfirst introducing the three programmes that dominated researchbetween the 1880s and the 1930s comparative experimental andhuman embryology I shall then review how the questions andapproaches scope and audiences of developmental biology made itdifferent from any of those Meetings funding journals societiescourses and textbooks defined the new speciality In the 1950s forthe first time when a colleague asked lsquoWhat do you dorsquo you couldanswer lsquoIrsquom a developmental biologistrsquo By the 1970s you couldexpect them to understand the response

Exceptions to my generalizations may come to mind I aim tosketch a big picture within which to place developmental biologynot to paint the detailed portrait that would need more historicalresearch Though I shall conclude by exploring the significance ofinclusion and exclusion today I have not published inDevelopmentfor over a quarter of a century (Hopwood et al 1992) Havingbecome a historian of science and medicine I know more aboutresearch on embryos in 1819 and 1919 than in 2019 So I shall notpresume to take a strong line on the present let alone the future butshall risk a few remarks about how thinking in terms of what is inand what is out might put strategies for renewal into perspective

Three embryologiesEmbryology was made a science in the decades around 1800 whenthe old anatomy and the broad framework of lsquogenerationrsquo beganto break down Teratology was established rather separately inthe same period Much research compared the development ofvertebrate embryos and analysed them in terms of germ layersand cells By the 1850s professors in the German universitieswere teaching medical students in dedicated courses Althoughtheir lectures and demonstrations nominally tackled lsquohumanembryologyrsquo the chick and domestic mammals provided much ofthe content especially for early stages For a long time embryologyhad no societies and seldom its own departments but evolutionismsoon drew attention to the science (Hopwood 2009)

Department of History and Philosophy of Science University of CambridgeFree School Lane Cambridge CB2 3RH UK

Author for correspondence (ndh12camacuk)

NH 0000-0001-7069-7497

1

copy 2019 Published by The Company of Biologists Ltd | Development (2019) 146 dev175448 doi101242dev175448

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ENT

From the 1860s Darwinists prized embryos as evidence ofcommon descent and ontogeny as an aid to constructingphylogenies (Gould 1977 Hopwood 2015) Comparativeembryology built much of the edifice of Darwinian biology as itinspired imperial safaris to bring home lsquoliving fossilsrsquo and lsquomissinglinksrsquo (Bowler 1996 Hall 2001) The most extremewas the lsquowinterjourneyrsquo of Robert Falcon Scottrsquos Antarctic expedition in 1911 Thebiologist EdwardWilson attached lsquothe greatest possible importancersquoto the embryology of the emperor penguin that lsquonearest approach toa primitive formhellipof a birdrsquo (Wilson 1907 p 31) He froze to deathwith Scott but a team-mate brought back three eggs ndash to a sadlyrather lukewarm reception (Raff 1996 pp 1-4)Evolutionists rarely claimed medical relevance embryology

was not in that sense a matter of life and death It was muchmore important than that at stake was where humanity camefrom why we are here and where we are going This gaveembryology public prominence for the first time Butembryologists comparative anatomists and palaeontologistsincreasingly disagreed on the relations of ontogeny and phylogenyand particularly the doctrine of recapitulation Their rancorousdisputes threw the field into crisis and by 1900 were driving youngresearchers away (Gould 1977 pp 167-206 Hopwood 2015pp 171-187) Comparative embryologists still innovated Forexample in 1911 they founded the first society for the science theInternational Institute of Embryology Members of this elitist clubcollected embryos of endangeredmammals in European colonies andproduced normal plates (Nieuwkoop 1961 Hopwood 2007) Yetafter World War I other research programmes made the runningled by experimental embryology or lsquodevelopmental mechanicsrsquo themost direct ancestor of developmental biologyFrom the 1880s Wilhelm Roux and other experimentalists had

asked not how organisms evolved but how in physiologicalterms one stage becomes the next especially how an egg turns into alarva or adult (Maienschein 1991 Nyhart 1995) That is a primeillustration of how questions about embryos have varied andchanged Developmental mechanics paid much attention toregulation and regeneration and had links to medicine forexample through the experimental generation of malformationsand claims to human rejuvenation (Maienschein 2011 Sengoopta2003) Plants were included in principle (Roux et al 1912) butplant embryology was more integrated into the rest of botany mostarticles in Rouxrsquos journal dealt with amphibia and marineinvertebrates In the early 20th century the approach wasconspicuous in the first centres for biology as distinct fromanatomy zoology or botany But the earliest specificallyembryological research institute focused on humansThat institute was the Department of Embryology at the Johns

Hopkins University in Baltimore which the Carnegie Institutionof Washington one of those private philanthropies that had begunto fund new fields founded in 1914 The Carnegie Departmentinstitutionalized themethods invented inGerman-speakingEurope ofcollaborating with clinicians to collect early human embryosthen analysing these by serial sectioning and plastic reconstruction(Hopwood20002002) Themissionwas anatomical andpathologicalndash to set up norms of development and explain deviations from them ndashand potential medical benefits helped justify support Evolution waslargely off the agenda and few experiments were possible TheCarnegie scientists instead concentrated on detailed descriptions ofhuman developmental anatomy eventually including the first twoweeks These fed intomedical teaching and are still used today (eg deBakker et al 2016) Between the world wars the department alsopioneered tissue culture studies of monkey embryology and

reproduction and cine films In the 1940s researchers there analysedthe results of early attempts to fertilize human eggs in vitro(Maienschein et al 2004 Buklijas and Hopwood 2008 Morgan2009 Marsh and Ronner 2008 pp 104-110)

Of the three research programmes ndash comparative experimentaland human ndash experimentation was dominant by the 1930s whenvarious new initiatives sprang up around it notably developmentalgenetics and chemical embryology (Keller 1986 Abir-Am 1994Fantini 2000) Hans Spemann and Hilde Mangoldrsquos discovery ofthe amphibian organizer was thrilling but failure to find out itsmode of action dampened the excitement considerably (Hamburger1988 Faumlszligler 1997) Embryology faced more general challenges bythe 1940s Especially in the USA it was separated from andthreatened by genetics which profited from its uses in breedingplants animals and humans (Gilbert 1998) In an age of striving forthe unity of science research on embryos was fragmented andmarginal On the eve of the massive postwar expansion ingovernment funding embryology was poorly placed to benefitDevelopmental biology might have been designed to solve theseproblems and to an extent it was

Defining developmental biologyThe expression lsquodevelopmental biologyrsquo first gained wide currencyin the postwar USA by then the major world power and pouringmoney into science Taking the lead Paul Weiss the emigreacuteAustrian Chicago professor and Chairman of the Division ofBiology and Agriculture at the National Research Council pushedthe National Science Foundation (NSF) to adopt the term In 1952the NSF replaced old divisions with a few categories that appliedacross the living world and so could integrate biology whileallowing support for medical research (Appel 2000 pp 63-66Brauckmann 2013 Crowe et al 2015) (Fig 1) In 1956 a series ofinternational meetings promoted the field (Weiss 1957 1958)Three years later when the journal Developmental Biology waslaunched with significant European input the subject was already agoing concern Practitioners traced this back to an importantincubator for the convergence between embryology and geneticsthe Society for the Study of Development and Growth renamed theSociety for Developmental Biology in 1965 (Oppenheimer 1966)(Table 1)

Weiss introduced the first issue of Developmental Biology bycalling on authors to unite the phenomena of lsquodevelopment andgrowthrsquo which had been dealt with in many disciplines from plantphysiology to oncology and included the lsquoseriation of stages ofchick embryosrsquo lsquonutrient control of bacterial growthrsquo and lsquorepair ofa broken bonersquo The processes of interest ranged from growthdifferentiation and morphogenesis through maturation and ageingregulation and regeneration Tackling these would requireengagement with lsquobroad problemsrsquo but Weiss otherwisecommitted to lsquodiversityrsquo and to accepting work lsquo[w]hetheranalytical or descriptive technical or theoretical whether using amolecular or an organismic approach whether dealing withmicroorganisms plants animals or manrsquo (Weiss 1959 furtherKeller 1995) Weiss claimed activities that had a place in Rouxrsquosgrandest plans for developmental mechanics but put more emphasisthan Rouxrsquos followers ever had in practice on embracing the wholeliving world including microbes

In that heyday of science funding by block grants developmentalbiologists found it fairly easy to claim applicability Weiss himselfhad worked during the war on nerve regeneration and evencontributed to surgical innovations A lsquogrowth and developmentrsquoperspective potentially illuminated numerous medical problems but

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fed into and drew most generally on cancer research which hadbeen prominent in the foundation of the Growth Society itself(Crowe 2014) It was widely accepted that lsquoorganizeddevelopmentrsquo lsquomay throw light uponrsquo lsquomalignant growthrsquo andvice versa (Berrill 1971 p 516)Inclusivity had its limits It is well known that developmental

biology also as established through textbooks and graduateprogrammes in the early 1970s excluded evolution and tended to

ignore the environment beyond the laboratory (but see eg Mintz1958) That was in part because the field followed experimentalembryology and in part because of the lure of biomedical dollars Itis less often noted that not only did lsquoembryologyrsquo mean somethingaltogether more traditional to generations of medical students andto some of their teachers but developmental biologists alsoorganized separately from reproductive biology This wasinstitutionalized around the same time but in laboratories linkedto farms clinics and population control (Clarke 1998) (Table 1)Mammalian developmental biologists moved between these worldshowever (and in Markert and Papaconstantinou 1975 the SDBembraced reproduction) In the 1970s embryo transfer was made anagricultural industry and in the 1980s in vitro fertilization became amedical one (Betteridge 2003 Henig 2004 Hopwood 2018b)

A few developmental biologists joined more medically orientedembryologists paediatricians and others in the teratology societiesthat were set up from 1960 initially in the USA and Japan Theseresponded to worries about congenital malformations ndash theirvisibility greater after World War II as mortality and morbidityfrom other causes declined ndash and attracted funding from a newHuman Embryology and Development Study Section of theNational Institutes of Health The thalidomide tragedy thenamplified their concerns (Kalter 2003 Dron 2016 furtherDonnai and Read 2003)

The UK like other countries which I cannot cover here made aless researched and apparently more gradual transition todevelopmental biology with much interaction across the Atlantic(Table 1) [For other countries see the special issues of theInternational Journal of Developmental Biology wwwijdbehueswebissuesspecial-countries] Young initiatives includingchemical embryology and developmental genetics had been wellrepresented in the UK since the 1930s But the LondonEmbryologistsrsquo Club the forerunner of the BSDB did not portrayitself as a disciplinary innovation when founded 71 years ago in1948 The minutes of the first meeting identified three useful buthardly revolutionary aims lsquo[i]nformal discussion of problems ofembryologyrsquo lsquomeet[ing] embryologists from other countriesrsquo andlsquocompil[ing] a record of research material in this countryrsquo (Slack2000) (Fig 2) Yet given the divisions between comparativeexperimental and human approaches it was novel just to bring themtogether (Hopwood 2009)

The London club encompassed all kinds of projects and a widerange of species including humans though not much explicitlycomparative work (Slack 2000) Research expanded anddiversified not least through the rise of molecular biology Theclub went national as the Society for Developmental Biology in1964 an obvious step although it is unclear why it was taken then

Fig 1 Annual totals in millions of dollarsby category for US federal grants andcontracts for unclassified research in thebasic life sciences for calendar year 1952(white) fiscal year 1954 (hatched) andfiscal 1955 (black) Detail reproduced withpermission from AAAS from Consolazio andJeffrey (1957) figure 2

Table 1 Years of foundation for selected organizations and journals ofdevelopmental biology and of reproductive biology andmedicine in theUSA and UK

Year Organization or journal

Developmental biologyUSA1939 Society for the Study of Development and Growth

rarr Society for Developmental Biology in 19651952 National Science Foundation program1956 Series of meetings1959 Developmental Biology1966 Current Topics in Developmental Biology

UK1948 London Embryologistsrsquo Club

rarr Society for Developmental Biology in 1964rarr British Society for Developmental Biology in 1969

1953 Journal of Embryology and Experimental Morphologyrarr Development in 1987

Reproductive biology and medicineUSA1944 American Society for the Study of Sterility

rarr American Fertility Society in 1965rarr American Society for Reproductive Medicine in 1995

1948 International Planned Parenthood Federation1950 Fertility and Sterility1955 Human Embryology and Development Study Section NIH1960 Teratology Society1967 Society for the Study of Reproduction1969 Biology of Reproduction1974 International Embryo Transfer Society

UK1944 Family Planning Association meetings

rarr Society for the Study of Fertility in 1949rarr Society for Reproduction and Fertility in 2001

1960 Journal of Reproduction and Fertilityrarr Reproduction in 2001

1985 European Society of Human Reproduction and Embryology (ESHRE)1986 Human Reproduction1993 Association of Clinical Embryologists

A more complete list would include the recent stem cell institutions (Forreproductive sciences see further Clarke 1998 pp 140-141)

3

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ENT

fed into and drew most generally on cancer research which hadbeen prominent in the foundation of the Growth Society itself(Crowe 2014) It was widely accepted that lsquoorganizeddevelopmentrsquo lsquomay throw light uponrsquo lsquomalignant growthrsquo andvice versa (Berrill 1971 p 516)Inclusivity had its limits It is well known that developmental

biology also as established through textbooks and graduateprogrammes in the early 1970s excluded evolution and tended to

ignore the environment beyond the laboratory (but see eg Mintz1958) That was in part because the field followed experimentalembryology and in part because of the lure of biomedical dollars Itis less often noted that not only did lsquoembryologyrsquo mean somethingaltogether more traditional to generations of medical students andto some of their teachers but developmental biologists alsoorganized separately from reproductive biology This wasinstitutionalized around the same time but in laboratories linkedto farms clinics and population control (Clarke 1998) (Table 1)Mammalian developmental biologists moved between these worldshowever (and in Markert and Papaconstantinou 1975 the SDBembraced reproduction) In the 1970s embryo transfer was made anagricultural industry and in the 1980s in vitro fertilization became amedical one (Betteridge 2003 Henig 2004 Hopwood 2018b)

A few developmental biologists joined more medically orientedembryologists paediatricians and others in the teratology societiesthat were set up from 1960 initially in the USA and Japan Theseresponded to worries about congenital malformations ndash theirvisibility greater after World War II as mortality and morbidityfrom other causes declined ndash and attracted funding from a newHuman Embryology and Development Study Section of theNational Institutes of Health The thalidomide tragedy thenamplified their concerns (Kalter 2003 Dron 2016 furtherDonnai and Read 2003)

The UK like other countries which I cannot cover here made aless researched and apparently more gradual transition todevelopmental biology with much interaction across the Atlantic(Table 1) [For other countries see the special issues of theInternational Journal of Developmental Biology wwwijdbehueswebissuesspecial-countries] Young initiatives includingchemical embryology and developmental genetics had been wellrepresented in the UK since the 1930s But the LondonEmbryologistsrsquo Club the forerunner of the BSDB did not portrayitself as a disciplinary innovation when founded 71 years ago in1948 The minutes of the first meeting identified three useful buthardly revolutionary aims lsquo[i]nformal discussion of problems ofembryologyrsquo lsquomeet[ing] embryologists from other countriesrsquo andlsquocompil[ing] a record of research material in this countryrsquo (Slack2000) (Fig 2) Yet given the divisions between comparativeexperimental and human approaches it was novel just to bring themtogether (Hopwood 2009)

The London club encompassed all kinds of projects and a widerange of species including humans though not much explicitlycomparative work (Slack 2000) Research expanded anddiversified not least through the rise of molecular biology Theclub went national as the Society for Developmental Biology in1964 an obvious step although it is unclear why it was taken then

Fig 1 Annual totals in millions of dollarsby category for US federal grants andcontracts for unclassified research in thebasic life sciences for calendar year 1952(white) fiscal year 1954 (hatched) andfiscal 1955 (black) Detail reproduced withpermission from AAAS from Consolazio andJeffrey (1957) figure 2

Table 1 Years of foundation for selected organizations and journals ofdevelopmental biology and of reproductive biology andmedicine in theUSA and UK

Year Organization or journal

Developmental biologyUSA1939 Society for the Study of Development and Growth

rarr Society for Developmental Biology in 19651952 National Science Foundation program1956 Series of meetings1959 Developmental Biology1966 Current Topics in Developmental Biology

UK1948 London Embryologistsrsquo Club

rarr Society for Developmental Biology in 1964rarr British Society for Developmental Biology in 1969

1953 Journal of Embryology and Experimental Morphologyrarr Development in 1987

Reproductive biology and medicineUSA1944 American Society for the Study of Sterility

rarr American Fertility Society in 1965rarr American Society for Reproductive Medicine in 1995

1948 International Planned Parenthood Federation1950 Fertility and Sterility1955 Human Embryology and Development Study Section NIH1960 Teratology Society1967 Society for the Study of Reproduction1969 Biology of Reproduction1974 International Embryo Transfer Society

UK1944 Family Planning Association meetings

rarr Society for the Study of Fertility in 1949rarr Society for Reproduction and Fertility in 2001

1960 Journal of Reproduction and Fertilityrarr Reproduction in 2001

1985 European Society of Human Reproduction and Embryology (ESHRE)1986 Human Reproduction1993 Association of Clinical Embryologists

A more complete list would include the recent stem cell institutions (Forreproductive sciences see further Clarke 1998 pp 140-141)

3

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The remit was lsquothose aspects of animal and plant biology that areconnected with developmental processesrsquo (SDB-1964 at bsdborg20180429bsdb-archive) To avoid confusion with the Americansociety which was renamed the next year the British one addedthe first lsquoBrsquo in 1969 The programme of the inaugural meeting ofthe national society hosted by John Gurdon in Oxford showsvaried interests biochemistry (proteins and DNA) andtransplantation plants and animals including humans and hydraand adult tissues as well as embryos (Fig 3) But neither evolutionnor environmental matters were represented any clinical relevancewas implicitThe Company of Biologists had founded the Journal of

Embryology and Experimental Morphology (JEEM) in 1953following an initiative of the International Institute in Utrecht as lsquoanew periodicalhellipprimarily devoted to morphogenesisrsquo Thecumbersome name signalled a pooling of resources forlsquoembryologistsrsquo like the London club more than anyreorganization of lsquothe science of developmentrsquo JEEM soughtlsquocontributionsrsquo about lsquohow living non-pathological structures arebuilt up increased maintained repaired [and] transformed either atthe supracellular or cellular or macromolecular levelrsquo With a focuson lsquothe animal realmrsquo and only lsquooccasional papers or reviewsrsquoexpected to lsquothrow out a bridge towards morphogenesis in unicellularand plant organismsrsquo (Dalcq 1953) the taxonomical scope wasnarrower than Developmental Biology or Current Topics inDevelopmental Biology By contrast JEEM was less exclusivelyexperimental biophysical and biochemical ndash and thus more opento for example descriptive human embryology ndash though it becamemore similar with its relaunch asDevelopment in 1987 (Wylie 2012)The BSDB and these journals were not the whole story because

society members wore various other hats As in the USA theestablishment of the reproductive sciences shaped these hybrididentities (Table 1) With the growing ability to culture mammalianembryos the large UK community of mammalian embryologistsplayed an increasing role in the BSDB and also attendedmeetings ofthe Society for the Study of Fertility (Graham 2000 Clarke 2007)Some have gone to conferences of the International EmbryoTransfer Society which is oriented towards animal breeding or theEuropean Society of Human Reproduction and Embryology which

has concentrated on IVF (Betteridge 2003 Brown 2005) Therewas and is mutual exclusion too the organization that claims withover 800 members to be lsquothe UKrsquos only professional bodyrepresenting embryologistsrsquo is not the BSDB but the Association ofClinical Embryologists (wwwembryologistsorguk last accessed 9November 2018)

Developmental biology may then consider itself the mainsuccessor of experimental embryology The somewhat separateinstitutionalization of embryos in reproductive biology andmedicine cautions against assuming that developmental biologymonopolized research after 1960 Like its principal predecessor ithas rather been one kind of embryology among several and with ascope for the most part more restricted even than Weissrsquos visionimplied

Golden agesDetailed historical investigation will be needed to establish theextent to which developmental biologists realized that visionExpansion surely made space for new areas of research fromnuclear transplantation through embryonal carcinoma andembryonic stem cells to plant systems But after 30 years lsquothegoal of easy discourse between animal and plant developmentalbiologists still seem[ed]rsquo to one American sea-urchin specialistlsquoonly on the horizonrsquo (Wilt 1990) In 1994 a celebration and stock-taking included lsquoall multicellular organismsrsquo but concentrated onthe core topics of embryogenesis morphogenesis and regeneration(Hines et al 1994) which had long been the focus ofdevelopmental biology textbooks too

Fig 3 Programme of the first meeting of the SDB inOxford 20 June 1964Reproduced with permission from the BSDB Archive John Innes CentreArchives Norwich

Fig 2 Minutes of the inaugural meeting of the London EmbryologistsrsquoClub at University College London on 2 March 1948 (detail) Reproducedwith permission from the BSDB Archive John Innes Centre ArchivesNorwich

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The initial advance of developmental biology was no simplelsquomolecularizationrsquo (Crowe et al 2015) but cells genes andmolecules did move centre stage as the control of gene expressionbecame the overriding interest The pull of genetics gavedevelopmental biology a different species profile from the oldexperimental embryology mice flies and worms were later joinedby thale cress and zebrafish In the 1980s the combination oftraditional but large-scale genetic and embryological methods withgene and antibody cloning produced an explosion of knowledgewhich I do not claim to represent fully with two journal covers(Fig 4) Problems set in the earlier 20th century were solved or theirsolution made to appear imminentThe field expanded on one measure from 690 researchers

internationally in 1949 to some 3400 in 1980 (Faber and Salomeacute1981) Membership of the BSDB rose from 186 in 1965 and 400 in1980 to 1246 in 2000 (BSDB Newsletter no 2 1980 p 2 1980-1(2) at httpbsdborg20180429bsdb-archive Slack 2000) Yetthe investment then necessary to carry out this sort of work reinforcedthe concentration on a few not entirely representative species (Bolker1995 but see also Davies 2007) Narrowing was a precondition ofdeepening and the advantages of exclusion of concentrating on eggto embryo in a handful of model organisms and a few experimentalsystems were well rehearsed In similar ways a tight focus hadallowed the Carnegie Department to describe human developmentalanatomy in exquisite detail and Spemannrsquos school to elucidate thebehaviour of the organizer though with diminishing returnsIn developmental biology a period of soul-searching followed

the excitement of the 1980s and 1990sWhen the field was foundedmoney had flowed and scientists enjoyed more freedom in researchthan ever before or since Calls for applications grew louder in the1970s and eventually reached developmental biology As fundersrequired pay-offs to justify higher levels of support all biologistsfelt more pressure to make the case (eg Gilbert 2017 Maartenset al 2018) [Knowing the amount of money available perdevelopmental biologist would define pressures that might have

favoured inclusion or exclusion but the era of model organismsshows that expansion and a certain narrowing could go hand inhand] It should be reassuring to remember that practical demandshave often driven fundamental discoveries such as in bacteriologyand immunology endocrinology and the control of reproduction(eg Oudshoorn 1994 Brock 1999)

Other challenges have been organizational technical andintellectual the welter of necessary but not always electrifyingdetail the stresses of fragmentation into competing subfields and thepolitics of species choice (Hopwood 2011) The difficulty ofnegotiating relations with the rapidly multiplying stem cell field hasloomed large amidst the hope horror and hype about regenerativemedicine (Maehle 2011 Maienschein 2011) Many developmentalbiologists have talked of lsquodeclinersquo from a lsquogolden agersquo (eg StJohnston 2015) though others and some of the same people see agilded present and a bright future (St Johnston 2015 Gilbert 2017Maartens and Tabin 2018 see also Pourquieacute 2012 2018 and Zon2019) With renewal in progress I hope that looking back will placerecent trends and aid reflection on the next paths to take

Strategies for renewalDevelopmental biologists have long drawn strength from embracingapproaches and methods of neighbouring fields The defaultstrategy is to include the latest techniques such as systemsanalysis based on lsquo-omicsrsquo and model-building gene editing andorganoids advanced imaging and soft-matter physics but to applythem to deepening core studies of embryogenesis (St Johnston2015) One of the most striking changes since I left the field is ageneral move to quantification with the mainstreaming ofmathematical modelling and routine interaction between lsquowetrsquo andlsquodryrsquo biology It is a source of optimism that new methods enlargethe range of options ndash inclusion and exclusion is not from a fixedmenu ndash but this is not enough On the one hand the postwarfounders of developmental biology enacted major exclusions thathave been relaxed as the costs have become clear On the other

Fig 4 Covers of Cell illustrate the successes and prominence of developmental biology in the late 1980s Left Weeks and Melton 1987 Right Drieverand Nusslein-Volhard 1988 Reprinted with permission from Elsevier

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SPOTLIGHT Development (2019) 146 dev175448 doi101242dev175448

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those early developmental biologists made promises aboutinclusion that are relevant stillThe founding promise was to study development across the living

world That sounds inclusive but researchersrsquo expectation that theprinciples would be the same in all multicellular organismsincreasingly justified their focus on just a few Interest in diversityfor its own sake goes back to the renaissance of lsquoevolution anddevelopmentrsquo around 1980 and gained momentum with thediscovery of the conserved colinearity of Hox genes and the riseof lsquoevo-devorsquo in the 1990s (Laubichler and Maienschein 2007)Since then it has been popular to go beyond model organisms tointroduce new ones and towork on several with less of a trade-off indepth than there used to be thanks to techniques such as RNAi andCRISPRCas (Hopwood 2011) Humans previously marginal todevelopmental biology have attracted renewed attention as stemcell cultures have opened differentiation and morphogenesis toexperimentation (Pourquieacute et al 2015)A second promise is less generally appreciated developmental

biology proposed to study the life course and not just egg to embryoor even sexual maturity Today more effort is going intounderstanding later processes from organogenesis throughhistogenesis to physiological function Developmental biologyhas played a role in ageing research not least in relation toprogrammed cell death (Jiang 2013) Looking to life cycles couldreduce the continuing separation from reproductive studies andmight help go further still The current ecological crisis makes acompelling argument for seeking a wider synthesis and researchincreasingly includes the environmental regulation of reproductionand development evolution and health (Gluckman et al 2010Gilbert and Epel 2015)

ConclusionsDevelopmental biology has not been just (experimental)embryology by another name Rather developmental biology wasmade after World War II with a particular set of inclusions andexclusions and has been reworked ever since By includingevolution and humans the field has now expanded to encompassversions of all three earlier embryologies that I picked out As youcontinue to remake it today you are including or excludingquestions and approaches species and audiences all the timeI have leant towards an inclusive strategy and pointed to

opportunities for example in reproduction and in ecology in theconviction that developmental biology will end up stronger andmore effective if it can succeed in tackling more But I accept that atalmost every historical juncture a commentator could haveemphasized either inclusion or exclusion as the productive moveMy brief is less for one vision or another and more for the value ofstanding back seeing the bigger picture and considering how itmatters what is kept in and what is left out

AcknowledgementsThe article is based on a talk at the 2018 BSDB Spring Meeting in Warwick I thankAndreas Prokop for the invitation to speak Aidan Maartens for commissioning thispiece Scott Gilbert Alex Gould Jeremy Green Tim Horder Martin Johnson AidanMaartens Alfonso Martinez Arias and two anonymous reviewers for comments ondrafts and Mike Taylor and Ian Bolton for scans

ReferencesAbir-Am P G (1994) The philosophical background of Joseph Needhamrsquos work inchemical embryology In A Conceptual History of Modern Embryology (ed S FGilbert) pp 159-180 Baltimore Johns Hopkins University Press

Appel T A (2000) Shaping Biology The National Science Foundation andAmerican Biological Research 1945ndash1975 Baltimore Johns Hopkins UniversityPress

Berrill N J (1971) Developmental Biology New York McGraw-HillBetteridge K J (2003) A history of farm animal embryo transfer and some

associated techniques Anim Reprod Sci 79 203-244Bolker J A (1995) Model systems in developmental biology BioEssays

17 451-455Bowler P J (1996) Lifersquos Splendid Drama Evolutionary Biology and the

Reconstruction of Lifersquos Ancestry 1860ndash1940 Chicago University of ChicagoPress

Brauckmann S (2013) Weiss Paul Alfred In Encyclopedia of Life SciencesChichester Wiley

Brock T D (1999) Robert Koch A Life in Medicine and Bacteriology WashingtonDC ASM Press

Brown S (2005) ESHRE The First 21 Years httpswwweshreeuHomeAbout-usHistory last accessed 25 January 2019

Buklijas T and Hopwood N (2008) Making Visible Embryos an onlineexhibition httpwwwhpscamacukvisibleembryos

Clarke A E (1998) Disciplining Reproduction American Life Sciences and lsquotheProblems of Sexrsquo Berkeley University of California Press

Clarke J (2007) The history of three scientific societies the Society for the Study ofFertility (now the Society for Reproduction and Fertility) (Britain) the SocieteFranccedilaise pour lrsquoEacutetude de la Fertilite and the Society for the Study ofReproduction (USA) Stud Hist Philos Biol Biomed Sci 38 340-357

Consolazio W V and Jeffrey H L (1957) Federal support of research in the lifesciences Science 126 154-155

Crowe N (2014) Cancer conflict and the development of nuclear transplantationtechniques J Hist Biol 47 63-105

Crowe N Dietrich M R Alomepe B S Antrim A F ByrneSim B L and HeY (2015) The diversification of developmental biology Stud Hist Philos BiolBiomed Sci 53 1-15

Cunningham A (2010) The Anatomist Anatomisrsquod An Experimental Discipline inEnlightenment Europe Farnham Ashgate

Dalcq A M (1953) Foreword J Embryol Exp Morphol 1 1-4Davies J A (2007) Developmental biologistsrsquo choice of subjects approximates to a

power law with no evidence for the existence of a special group of lsquomodelorganismsrsquo BMC Dev Biol 7 40

de Bakker B S de Jong K H Hagoort J de Bree K Besselink C T deKanter F E C Veldhuis T Bais B Schildmeijer R Ruijter J M et al(2016) An interactive three-dimensional digital atlas and quantitative database ofhuman development Science 354 aag0053

Donnai D and Read A P (2003) How clinicians add to knowledge ofdevelopment Lancet 362 477-484

Driever W and Nusslein-Volhard C (1988) The bicoid protein determinesposition in the Drosophila embryo in a concentration-dependent manner Cell 5495-104

Dron H A (2016) Teratology transformed uncertainty knowledge and conflictover environmental etiologies of birth defects in midcentury America PhDdissertation History of Health Sciences University of California San Francisco

Faber J and Salome B Z (1981) Introduction Gen Embryol Inf Service 18 4Faszligler P E (1997) Hans Spemann 1869ndash1941 Experimentelle Forschung im

Spannungsfeld von Empirie und Theorie Ein Beitrag zur Geschichte derEntwicklungsphysiologie zu Beginn des 20 Jahrhunderts Berlin Springer

Fantini B (2000) Lrsquoembryologie la lsquogeographie chimiquersquo de la cellule et lasynthe se entre morphologie et chimie (1930ndash1950) Hist Philos Life Sci 22353-380

Gilbert S F (1998) Bearing crosses a historiography of genetics and embryologyAm J Med Genet 76 168-182

Gilbert S F (2017) Developmental biology the stem cell of biological disciplinesPLoS Biol 15 e2003691

Gilbert S F and Epel D (2015) Ecological Developmental Biology TheEnvironmental Regulation of Development Health and Evolution 2nd ednSunderland MA Sinauer

Gluckman P D Hanson M A and Buklijas T (2010) A conceptual frameworkfor the developmental origins of health and disease J Dev Orig Health Dis1 6-18

Gould S J (1977) Ontogeny and Phylogeny Cambridge MA Harvard UniversityPress Belknap Press

Graham C (2000) Mammalian development in the UK (1950ndash1995) Int J DevBiol 44 51-55

Hall B K (2001) John Samuel Budgett (1872ndash1904) in pursuit of PolypterusBioscience 51 399-407

Hamburger V (1988) The Heritage of Experimental Embryology Hans Spemannand the Organizer New York Oxford University Press

Henig R M (2004) Pandorarsquos Baby How the First Test Tube Babies Sparked theReproductive Revolution Boston Houghton Mifflin

Hines P J Marx J and Parks S (1994) Frontiers in development Science 266523

Hopwood N (2000) Producing development the anatomy of human embryos andthe norms of Wilhelm His Bull Hist Med 74 29-79

6

SPOTLIGHT Development (2019) 146 dev175448 doi101242dev175448

DEVELO

PM

ENT

Hopwood N (2002) Embryos in Wax Models from the Ziegler Studio with aReprint of lsquoEmbryological Wax Modelsrsquo by Friedrich Ziegler Cambridge WhippleMuseum of the History of Science Bern Institute of the History of Medicine

Hopwood N (2007) A history of normal plates tables and stages in vertebrateembryology Int J Dev Biol 51 1-26

Hopwood N (2009) Embryology In The Cambridge History of Science vol 6 TheModern Biological and Earth Sciences (ed P J Bowler and J V Pickstone)pp 285-315 Cambridge Cambridge University Press

Hopwood N (2011) Approaches and species in the history of vertebrateembryology In Vertebrate Embryogenesis Embryological Cellular and GeneticMethods Methods in Molecular Biology vol 770 (ed F J Pelegri) pp 1-20New York Humana Press

Hopwood N (2015) Haeckelrsquos Embryos Images Evolution and Fraud ChicagoUniversity of Chicago Press

Hopwood N (2018a) The keywords lsquogenerationrsquo and lsquoreproductionrsquo InReproduction Antiquity to the Present Day (ed N Hopwood R Flemming andL Kassell) pp 287-304 Cambridge Cambridge University Press

Hopwood N (2018b) Artificial fertilization In Reproduction Antiquity to thePresent Day (ed N Hopwood R Flemming and L Kassell) pp 581-596Cambridge Cambridge University Press

Hopwood N D Pluck A Gurdon J B and Dilworth S M (1992) Expressionof XMyoD protein in early Xenopus laevis embryos Development 114 31-38

Horder T (2010) History of developmental biology In Encyclopedia of LifeSciences Chichester Wiley

Jacob F (1982) The Logic of Life A History of Heredity trans Betty E SpillmannNew York Pantheon

Jiang L (2013) Degeneration in miniature history of cell death and aging researchin the twentieth century PhD dissertation Arizona State University

Kalter H (2003) Teratology in the 20th century environmental causes ofcongenital malformations in humans and how they were establishedNeurotoxicol Teratol 25 131-282

Keller E F (1986) Drosophila embryos as transitional objects the work of DonaldPoulson and Christiane Nusslein-Volhard Hist Stud Nat Sci 26 313-346

Keller E F (1995) Refiguring Life Metaphors of Twentieth-Century BiologyNew York Columbia University Press

Laubichler M D and Maienschein J (ed) (2007) From Embryology toEvo-Devo A History of Developmental Evolution Cambridge MA MIT Press

Lenoir T (1997) Instituting Science The Cultural Production of ScientificDisciplines Stanford Stanford University Press

Maartens A and Tabin C (2018) An interview with Cliff Tabin Development 145dev161638

Maartens A Prokop A Brown K and Pourquie O (2018) Advocatingdevelopmental biology Development 145 dev167932

Maehle A-H (2011) Ambiguous cells the emergence of the stem cell concept inthe nineteenth and twentieth centuries Notes Rec R Soc Lond 65 359-378

Maienschein J (1991) Transforming Traditions in American Biology 1880ndash1915Baltimore Johns Hopkins University Press

Maienschein J (2011) Regenerative medicinersquos historical roots in regenerationtransplantation and translation Dev Biol 358 278-284

Maienschein J Glitz M and Allen G E (ed) (2004) Centennial History of theCarnegie Institution of Washington vol 5 The Department of EmbryologyCambridge Cambridge University Press

Markert C L and Papaconstantinou J (ed) (1975) The Developmental Biologyof Reproduction Symposia of the Society for Developmental Biology vol 33New York Academic Press

Marsh M and Ronner W (2008) The Fertility Doctor John Rock and theReproductive Revolution Baltimore Johns Hopkins University Press

Martinez Arias A (2013) Stem cells in developmental biology a debate at theBSDB 25 March httpamapressgencamacukp=996

Mintz B (ed) (1958) Environmental Influences on Prenatal Development TheDevelopmental Biology Conference Series 1956 Chicago University of ChicagoPress

Morgan L M (2009) Icons of Life ACultural History of Human Embryos BerkeleyUniversity of California Press

Nieuwkoop P D (1961) lsquoLrsquoInstitut International drsquoEmbryologiersquo (1911ndash1961)GenEmbryol Inf Service 9 265-269

Nyhart L K (1995) Biology Takes Form Animal Morphology and the GermanUniversities 1800ndash1900 Chicago University of Chicago Press

Oppenheimer J M (1966) The growth and development of developmentalbiology InMajor Problems in Developmental Biology Symposia of the Society forDevelopmental Biology vol 25 (ed M Locke) pp 1-27 New York AcademicPress

Oudshoorn N (1994) Beyond the Natural Body An Archeology of Sex HormonesLondon Routledge

Pourquie O (2012) Development looking to the future Development 1391893-1894

Pourquie O (2018) And one last thing Development 145 dev162446Pourquie O Bruneau B Keller G and Smith A (2015) Looking inwards

opening a window onto human development Development 142 1-2Raff R A (1996) The Shape of Life Genes Development and the Evolution of

Animal Form Chicago University of Chicago PressRoux W Correns C Fischel A and Kuster E (1912) Terminologie der

Entwicklungsmechanik der Tiere und Pflanzen Leipzig EngelmannSengoopta C (2003) lsquoDr Steinach coming to make old youngrsquo sex glands

vasectomy and the quest for rejuvenation in the roaring twenties Endeavour 27122-126

Slack J M W (2000) A short history of the British Society for DevelopmentalBiology Int J Dev Biol 44 79-83

St Johnston D (2015) The renaissance of developmental biology PLoS Biol 13e1002149

Weeks D L and Melton D A (1987) A maternal mRNA localized to the vegetalhemisphere in Xenopus eggs codes for a growth factor related to TGF-β Cell 51861-867

Weiss P (1957) Developmental biology Science 126 708-712Weiss P (1958) Preface to the series In The Developmental Biology Conference

Series 1956 Embryonic Nutrition (ed D Rudnick) pp v-viii Chicago Universityof Chicago Press

Weiss P (1959) Introduction Dev Biol 1 i-iiiWilson E A (1907) Aves In National Antarctic Expedition 1901ndash1904 section 1

Natural History vol 2 Zoology (Vertebrata Mollusca Crustacea) London BritishMuseum

Wilt F H (1990) Thirty years of Developmental Biology a growth industry DevBiol 141 241-242

Wylie C (2012) In the beginning Development 139 1889-1890Zon L (2019) Improving the visibility of developmental biology time for induction

and specification Development 146 dev174631

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SPOTLIGHT Development (2019) 146 dev175448 doi101242dev175448

DEVELO

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ENT