Approaches and species in the history of vertebrate embryology.
ABSTRACT Recent debates about model organisms echo far into the past; taking a longer view adds perspective to present concerns. The major approaches in the history of research on vertebrate embryos have tended to exploit different species, though there are long-term continuities too. Early nineteenth-century embryologists worked on surrogates for humans and began to explore the range of vertebrate embryogenesis; late nineteenth-century Darwinists hunted exotic ontogenies; around 1900 experimentalists favored living embryos in which they could easily intervene; reproductive scientists tackled farm animals and human beings; after World War II developmental biologists increasingly engineered species for laboratory life; and proponents of evo-devo have recently challenged the resulting dominance of a few models. Decisions about species have depended on research questions, biological properties, supply lines, and, not least, on methods. Nor are species simply chosen; embryology has transformed them even as they have profoundly shaped the science.
Final author manuscript for Chapter 1 of Vertebrate Embryogenesis: Embryological,
Cellular, and Genetic Methods (Methods in Molecular Biology 770), ed. Francisco J.
Pelegri (New York: Humana Press), pp. 1–20. The final publication is available at
Approaches and Species in the History of Vertebrate Embryology
Recent debates about model organisms echo far into the past; taking a longer
view adds perspective to present concerns. The major approaches in the history of
research on vertebrate embryos have tended to exploit different species, though there
are long-term continuities too. Early nineteenth-century embryologists worked on
surrogates for humans and began to explore the range of vertebrate embryogenesis;
late nineteenth-century Darwinists hunted exotic ontogenies; around 1900
experimentalists favored living embryos in which they could easily intervene;
reproductive scientists tackled farm animals and human beings; after World War II
developmental biologists increasingly engineered species for laboratory life; and
proponents of evo-devo have recently challenged the resulting dominance of a few
models. Decisions about species have depended on research questions, biological
properties, supply lines and, not least, on methods. Nor are species simply chosen;
embryology has transformed them even as they have profoundly shaped the science.
Key Words: Developmental biology; embryology; evo-devo; history; methods;
model organisms; species choice.
Running Title: History of Approaches and Species
1. Species Choice
Species choice has recently become prominent and controversial in debates
over the pros and cons of the dominant “model organisms” in developmental biology
(1). New systems seem to be announced almost monthly and laboratories are now
more likely to cross species boundaries too. While this volume aims to promote that
shift, this chapter puts these changes into historical perspective.
Embryologists have chosen organisms for their medical, agricultural, fisheries,
sporting or other practical importance, or because they were considered biologically
special. They have worked on surrogates for the species of most interest, especially
humans, and on convenient representatives of groups (2). Different kinds of
embryology have exploited various vertebrates in contrasting ways. Late nineteenth-
century evolutionists, for example, risked life and limb on expeditions to hunt
phylogenetically strategic embryos for histology. Twentieth-century experimentalists
chose accessible organisms that would provide abundant living, easily analysed
embryos on demand.
The histories of such models as chick, Xenopus, mouse and zebrafish show
that species selection never simply matches research questions and biological
properties. It is also about a community’s values, institutions, networks and
techniques: the kind of research it admires, the supply lines it can set up, the methods
it can develop and, increasingly, the features it can engineer (3,4,5,6,7,8,9). So species
are not simply chosen for embryology. Complex experiments need elaborate
infrastructures around highly domesticated organisms, but even to produce the most
basic description embryos have to be seen within a developmental frame. It is easy to
take this for granted today; historically, it was necessary to set up standard series and
to challenge competing interpretations by other people (10,11).
Species choice creates opportunities and sets limits that strongly shape
research (1). Competing research programmes invest in rival organisms (12,13);
scientists bet on which organism–problem combination will prove most productive;
agencies fund one rather than another. This is now clear for particular organisms and
episodes, especially in the later twentieth and early twenty-first centuries, but the
overall pattern is only starting to come into view. The chapter introduces the major
approaches in the history of research on vertebrate embryos (14) and shows, in broad
outline, why and how they have exploited different organisms. It begins to survey the
long-term politics of species choice in embryology. (See Note 1.)
2. Histories of Development
Philosophers and physicians had for centuries investigated the generation of
various animals and especially the chick, because its large eggs were abundantly
available as food. But only in the age of revolutions around 1800 was embryology
made a separate science. Developing embryos were framed as the objects of interest
by rejecting older views, for example, of the acquisition of a rational soul as the
crucial event in human pregnancy, and by using new techniques. Especially in
German university institutes of anatomy and physiology, microscopists explored how
complex bodies develop from simple beginnings. Through the mid-1800s they
collected and dissected specimens, preserved them in spirits of wine, and observed
and drew them through increasingly effective microscopes. They set up
developmental series, correcting times for temperature where they could, and
selecting representatives against which to assess new finds. They analysed embryos
into germ layers and cells. Copper plates or lithographs accompanied the most
prestigious publications (Fig. 1).
Medical and anthropological interest focused on humans, but anatomists had
to rely on encounters with aborting women and the occasional post mortem. So
embryos were inaccessible for about the first fortnight and rare for the next few
weeks. Suspicions of abnormality made it hard to have confidence in accounts of
normal development. Conveniently then, the most exciting comparative discoveries,
such as the 1825 announcement of “gills in mammals” (16), reinforced the
assumption that, across all the vertebrates, early development was fundamentally the
same. So researchers fished amphibian spawn out of ponds, warmed hen’s eggs in
artificial incubators, and bought and bred rabbits and dogs. Physiologists criticized
those who concentrated on human material they saw as uninformative. “[T]he history
of the bird embryo is … the ground on which we march forward,” while “that of the
mammalian fetus is the guiding star, which promises us safety on our route towards
the development of man” (17).
Yet embryologists also hoped that embryos would reveal the true relations
between groups more clearly than in later life, and thus help comparative anatomy to
produce a natural classification. To explore the play of difference within the
underlying unity, they collected viper eggs, acquired deer from hunters, and obtained
the conveniently transparent teleost embryos by artificial fertilization (5,18,19).
Dealers supplied occasional exotics, and when Louis Agassiz emigrated from
Switzerland to the United States in 1846 he opened up the American fauna, notably
fishes and turtles, for comparative embryology (20). Embryologists were few, though,
and the biological, geographical and social obstacles were large. A major survey of
1881 still identified huge gaps (21)—but by then things were beginning to change.
3. Ontogeny, Phylogeny and Histology
Darwinism drew on embryology for some of the strongest and most detailed
evidence for common descent. From the late 1860s, with the slogan “ontogeny
recapitulates phylogeny,” the German zoologist Ernst Haeckel raised its profile in the
universities and among the general public (22,23). He also changed its species
politics. Nothing had been so damaging, he controversially declared, as concentration
on the development of the chick. This had suffered such major changes from the
ancestral form of the vertebrates—it was, in Haeckel’s terminology, so
“cenogenetic”—as to give a wholly misleading view. Embryology should start again
should start again from the acraniate amphioxus and systematically pursue
comparative research (24). While teaching focused on a few types, usually including
the chick (25), he encouraged embryologists to discover the origins of the vertebrates,
of tetrapods, and especially of human beings.
Land-locked European researchers, most of them pursuing careers as
professors of anatomy or of zoology, created new institutions and exploited imperial
networks to gain access to the rest of the world (26). Marine stations made it possible
to utilize the sea more efficiently. Haeckel’s student Anton Dohrn founded the most
important in 1872 at Naples, where the Russian Alexander Kovalevsky had already
influentially explored the development of ascidians and amphioxus and significant
work on elasmobranchs would be done (27,28,29). Embryologists took advantage of
an increasingly global web of collectors, for example, to establish a breeding colony
of opossums, an American marsupial, in Bavaria (30).
The most intrepid scientists set sail to bring home “living fossils” and
“missing links.” They expected to find evidence of the major transitions most
faithfully preserved in the early embryos of these groups. They caught lungfish spawn
and other documents of tetrapod origins in South America, West Africa and the
Australian bush (11,31), which also provided embryos of monotremes (egg-laying
mammals): the platypus (26) and the spiny anteater or echidna. Colonial officials and
settler farmers gave another Haeckel student Richard Semon access to echidna
country and helped recruit native Australians. They staffed his camp and collected the
nocturnal anteaters that lived, shyly and quietly, in the most impenetrable bush. Many
settlers had never seen one, but the “incomparable nose and hawk’s eye” of “the
blacks” could follow the slight and complex tracks over difficult terrain to the hollows
where the animals slept by day (Fig. 2). So they were cross when Semon paid little or
nothing for the more numerous males (32). Many females were also sacrificed in vain.
He had to preserve specimens on the spot, and because the aborigines returned at
dusk, often ended up dissecting uterine embryos out of their tight-fitting shells “by the
light of a flickering candle” (33).
The explorers valorized their own derring-do, and excused the gaps in their
collections, by presenting rabbit breeding as tame (33). Yet another of Haeckel’s
students, Willy Kükenthal, accompanied whalers in the Northern seas, but found it
hard to intervene during the freezing storms on the ships, where everything had to
happen fast. He did better at the processing stations in Spitsbergen (34). The Erlangen
Darwinist Emil Selenka’s hunting trips to the East Indies laid the foundations of the
embryology of apes. But he lost rare treasures in a boat collision and was so sick with
malaria that his wife Lenore had to make good the loss (35). The most arduous, and
among the least successful, embryological collecting was of emperor penguin eggs
during the fateful “winter journey” of Robert Falcon Scott’s Antarctic expedition in
1911. Working out the embryology of “the nearest approach to a primitive form not
only of a penguin, but of a bird” had seemed “a matter of the greatest possible
importance,” and cost biologist Edward A. Wilson his life, but sadly, no one much
cared about the three fairly late-stage eggs that made it back (36,37).
Collecting worked profound intellectual transformations. This is because it
framed materials as embryos that the suppliers had often interpreted in other terms.
The aborigines knew how to track the echidna, or “cauara,” because it was a prized
delicacy; they also told Semon of its origin from a bad man who was filled with
spears. He impressed “the bushmen” by showing that the young were not “conceived
on the teat,” as they had believed, but began, like other mammals, in the womb (32).
Some of the deepest transformations went on closest to home. Even women who
knew they were pregnant—and in the early stages, especially before hormonal tests,
many did not—rarely interpreted the blood clots they passed in embryological terms.
Depending on whether or not a woman desired a pregnancy, she might think in terms
of a child to come or of waste material that had to be removed. Anatomists
appropriated bleeds that had been experienced variously as unremarkable late periods,
distressing miscarriages or desired restorations of menstrual flow (10).
Embryos of different species were then made equivalent by analysing them in
comparable ways. The great innovation of the 1870s was routine serial sectioning
with microtomes to give more detailed access to internal forms than dissection could
achieve. Though embryos were sometimes observed fresh using low-power
microscopes and drawing apparatus, sectioning became central to embryological
technique. Once obtained, and sometimes cultured, the material was fixed and stained,
embedded and cut by methods adapted to each taxonomic group and stage (38,39).
For particularly complex forms it became common to reconstruct three-dimensional
views from the sections, either graphically or in wax (40).
Debates over evolution made degrees of similarity and difference so contested
that other vertebrates could no longer stand in for human embryos. Haeckel’s leading
critic, the Swiss anatomist Wilhelm His, reformed the field by applying the
microtome to a rich supply of precious human specimens from the third week to the
end of the second month. Since he could not set up rigorous stages for this scarce and
variable material, he invented a ‘normal plate’ that simply arranged representative
specimens in series (10).
Anatomists now prided themselves on studying human embryos directly. In
1914 they established this non-evolutionary human embryology, primarily using
material recovered during surgery, by founding the Carnegie Institution of
Washington Department of Embryology at the Johns Hopkins University (41,42,43).
A primate colony was installed there in the 1920s (44). (Today the human embryo
collection is at the National Museum of Health and Medicine in Washington, D.C.)
Meanwhile, as evolutionists increasingly questioned Haeckel’s doctrine of
recapitulation, high-profile disagreements sent the field into crisis (11,22,45). To
reassess the relations between ontogeny and phylogeny, the German anatomist Franz
Keibel organized an international series of 16 vertebrate normal plates (11) (Fig. 3).
The revived comparative studies were institutionalized in 1911 in the International
Institute of Embryology. Constituted through a series of meetings in different
locations, this club promoted ‘salvage’ embryology: collecting endangered colonial
mammals for what became the Central Embryological Collection at the Hubrecht
Laboratory in Utrecht (47). (It was transferred in 2004 to the Natural History Museum
in Berlin.) Evolutionary embryology nevertheless declined after World War I, and
experimentalists disparaged comparative work as merely “descriptive.”
4. Experimental Cultures
From the 1880s, some embryologists took a radically different approach,
reconstructing embryology not as a historical science but on the model of the new
experimental physiology with its ideal of controlling life. Occasional earlier
experiments had generated additional forms to anatomize and taxonomize, but now
the focus was less on evolutionary questions than on how, in the present, one stage
produced the next.
The anatomist Wilhelm Roux and other exponents of “developmental
physiology” or “developmental mechanics” employed a range of interventions,
mechanical (shaking, cutting, constricting, pressure, gravity, centrifugal force),
thermal, chemical and electrical. The pioneers tended to use small metal scissors,
needles and knives; in the next generation zoologist Hans Spemann’s microsurgery
relied on hair loops and much finer glass instruments that he made himself (48) (Fig.
4). The new stereomicroscopes allowed finer manipulations (50), but careful culture
was at least as important as fancy apparatus, especially since antibiotics came in, for
the more challenging cultures, only after World War II. Keibel’s elaborate normal
plates were condensed into diagnostic “normal stages” (11). “Fate maps” used vital
dyes to show what early regions would become (51). Grafts were also marked by
species differences in pigmentation.
Species here mattered little for their own sakes. So fishes tended to lose out,
because researchers no longer much cared about either their extraordinary diversity or
their position as basal vertebrates, while other classes provided living embryos that
were more easily cultured and manipulated in large numbers (5). Among the
vertebrates the freely accessible, large and extremely resilient eggs of local Amphibia
were much the most popular for extirpation, explantation and transplantation, with
chicks in second place (49,52,53). Relevant work on mammals went on in the new
field of reproductive science (54). The pig was used in teaching alongside the chick.
Embryologists had always specialized in certain groups, but never as much as
Spemann, co-discoverer of the organizer. He arranged his career and those of almost
all his students and collaborators around microsurgical work on species of the
salamander Triton (now mostly Triturus). This concentration shows the shape of
things to come, but the breeding season still limited the experiments to the spring
5. Model Organisms
After World War II, massively expanded government funding allowed
biological and especially biomedical research to expand and intensify. Seeking the
most productive experimental systems, biologists and especially geneticists focused
on a few readily available model organisms. With their short generation times, small
adult sizes, and general suitability for laboratory domestication, these species would
dominate research on development.
Evolution was sidelined as the new “developmental biology” studied cellular,
molecular and genetic processes, and increasingly patterns and mechanisms of gene
expression, in the most convenient organisms. Comparative research continued in
traditional departments, museums, marine stations and fisheries labs (57), and
experiments used a wide variety of embryos (see Note 2). But just a few species
account for most of the big growth in developmental biology (58,59). The fruitfly