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OUP CORRECTED AUTOPAGE PROOFS – FINAL, 28/05/21, SPi
TH E
GENE’S -E Y E
V I EW OF
EVOLUTION
by
J. A RV I D ÅGR E N
Wenner-Gren Fellow
Department of Organismic and
Evolutionary Biology
Harvard University
1
OUP CORRECTED AUTOPAGE PROOFS – FINAL, 04/06/21, SPi
1
Great Clarendon Street, Oxford, ox2 6dp,
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© J. Arvid Ågren 2021
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First Edition published in 2021
Impression: 1
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DOI: 10.1093/oso/9780198862260.001.0001
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OUP CORRECTED AUTOPAGE PROOFS – FINAL, 28/05/21, SPi
For
my father, the biologist
and
my mother, the cultural historian
OUP CORRECTED AUTOPAGE PROOFS – FINAL, 28/05/21, SPi
OUP CORRECTED AUTOPAGE PROOFS – FINAL, 28/05/21, SPi
Preface
x Pr e face
that I for the first time came in close contact with students from
North America. One thing that struck me about my new colleagues
was that they often had a very different perspective on theoretical
issues in evolutionary biology than I did. To exaggerate and overgen-
eralize a bit: if when I was a teenager and expressed an interest in the
big questions of evolutionary biology I was handed a book authored
by Richard Dawkins, they had been given one of Stephen Jay Gould’s.
I learned a tremendous amount discussing these issues in the lecture
halls, seminar rooms, and, especially, in the Graduate Student Union
pub located right next to the Department of Ecology and Evolutionary
Biology of the University of Toronto. The genesis of this book owes
a lot to those intellectual sparring sessions.
More concretely, several people were instrumental in making this
book a reality. In particular, David Haig, and his Fundamental
Interconnectedness of All Things discussion group, provided an environ-
ment that encouraged tackling the foundational questions of our field.
Few have thought more about the gene’s-eye view than David and he
has been reliable source of advice and support throughout this project.
I am grateful a large number of colleagues who took the time to read
and provide comments on my writing. For help with individual chap-
ters, I thank Alan Grafen, Alister McGrath, Andrew Bourke, Anthony
Edwards, Cédric Paternotte, Charles Goodnight, Dan Dennett, Dan
Hartl, Denis Noble, Ellen Clarke, Erik Svensson, Jack Werren, Jim
Mallett, John Durant, Jonathan Birch, Kevin Foster, Lutz Fromhage,
Megan Frederickson, Michael Bentley, Michael Rodgers, Stephen
Wright, Stu West, and Tim Lewens. Others, including David Barash,
Brian and Deborah Charlesworth, Andy Clark, James Marshall, and
Martin Nowak, answered questions and pointed me to resources that
have been tremendously helpful. For reading the entire manuscript, at
one point or another, I am indebted to Chinmay Sonawane, Cody
McCoy, David Haig, Jon Ågren, Manus Patten, Richard Dawkins, Samir
Okasha, Steve Stearns, and Tobias Uller.
Their comments greatly improved the text, clarified my thinking,
and offered much needed encouragement. On occasion, they also saved
OUP CORRECTED AUTOPAGE PROOFS – FINAL, 28/05/21, SPi
Pr e face xi
Contents
xiv Con t e n ts
References 195
Index235
OUP CORRECTED AUTOPAGE PROOFS – FINAL, 04/06/21, SPi
The Gene’s-Eye View of Evolution. J. Arvid Ågren, Oxford University Press. © J. Arvid Ågren 2021.
DOI: 10.1093/oso/9780198862260.003.0001
OUP CORRECTED AUTOPAGE PROOFS – FINAL, 28/05/21, SPi
heritable traits, and if any of them make the individual more likely to
survive and reproduce, these traits will become more common in the
population as the generations go by. The gene’s-eye view represents a
subtle but radical shift in perspective. Building on the insight from
population genetics that evolutionary change can be described as the
increase or decrease of certain genetic variants, it argues that evolu-
tion is best thought of from the perspective of genes. By this reason-
ing, organisms are nothing but temporary occurrences—present in
one generation, gone in the next. And, as a consequence, organisms
cannot be the ultimate beneficiary in evolutionary explanations.
Instead, this role is filled by the gene. Genes are considered immor-
tal and they pass on their intact structure from generation to gener
ation. This way of thinking is also called selfish gene thinking, because
natural selection is conceptualized as a struggle between genes, usually
through the effects they have on organisms, for replication and trans-
mission to the next generation. Here, ‘genes’ is used in a somewhat lax
way. The evolutionary struggle is not between different genes within
the same organism (though, as will become clear, the gene’s-eye view
offers a powerful way to think about such genetic conflicts) but
between different alleles of the same gene within a population.
The origin of the gene’s-eye view involved many people, but two
stand above the rest: the American George C. Williams (1926–2010)
and the Brit Richard Dawkins (1941–). The idea was first explicitly
laid out by Williams in Adaptation and Natural Selection (Williams 1966),
and then 10 years later more forcefully by Dawkins in The Selfish Gene
(Dawkins 1976). Few phrases in science have caught the imagination
of laypeople and professionals alike the way that ‘selfish gene’ has
done, and it changed how both groups thought about evolution and
natural selection. Among both groups, the gene’s-eye view, has subse-
quently amassed both strong supporters and fierce critics.
The debate over the value of the gene’s-eye view has raged for over
half a century. It has pitted 20th century Darwinian aristocrats such as
John Maynard Smith and W.D. Hamilton against Richard Lewontin
and Stephen Jay Gould in the pages of Nature as well as those of The
OUP CORRECTED AUTOPAGE PROOFS – FINAL, 28/05/21, SPi
New York Review of Books. Even today, commentators cannot agree. For
example, in 2015 when the science historian Nathaniel Comfort
reviewed the second volume of Dawkins’s autobiography for Nature he
referred to the gene’s-eye view as ‘looking increasingly like a twentieth-
century construct’ (Comfort 2015). In contrast, writing for the same
journal only a few months later, the biologist turned journalist and
businessman Matt Ridley concluded that ‘no other explanation [for
evolution] makes sense’ (Ridley 2016). Professional biologists remain
equally divided. Simon Conway Morris dismissed it as ‘an exploded
concept that was almost past its sell-by date as soon as it was popular-
ized’ (Conway Morris 2008, p. ix). Similarly, a senior colleague of mine
who I showed an early draft of this manuscript wondered if he really
would be a suitable person to provide feedback as he disagreed with
‘virtually every aspect of the field’ and as a result he has ‘trouble separat-
ing their bad science from good faith attempts to describe it’. Yet,
Andy Gardner called The Selfish Gene ‘unequivocally the most
important popular book on evolutionary biology of the 20th century’
(Gardner 2016), a view shared by the Royal Society who in July 2017
announced that, after a public poll, The Selfish Gene had been voted
‘the most inspiring science book of all time’.
Much of the discomfort over the gene’s-eye view comes from its sur-
rounding vocabulary. Genes are ‘selfish’, organisms mere ‘survival
machines’, and bodies nothing but ‘lumbering robots’. The philosopher
Roger Scruton complained that these ideas made ‘cynicism respectable
and degeneracy chic’ (Scruton 2017, p. 49). Along these lines, a com-
monly told story (meaning it is seemingly impossible to track down
the original source) is that The Selfish Gene was the favourite book of
the disgraced Enron CEO Jeffrey Skilling, and that he used the book
to justify the exploitative cutthroat culture of the company.
But the debate over the gene’s-eye view is about so much more.
It overthrows our conception of familiar biological terms like gene,
fitness, and organism. It brings to the forefront evolutionary biologists’
peculiar habit of speaking of biological entities as having intentions,
deploying strategies, and pursuing goals. It drills to the core of what
OUP CORRECTED AUTOPAGE PROOFS – FINAL, 28/05/21, SPi
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