vol. 174, supplement
the american naturalist
The Evolutionary Enigma of Sex
Sarah P. Otto
Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada
Sexual reproduction entails a number of costs, and yet
the majority of eukaryotes engage in sex, at least occasionally. In this
article, I review early models to explain the evolution of sex and why
they failed to do so. More recent efforts have attempted to account
for the complexities of evolution in the real world, with selection
that varies over time and space, with differences among individuals
in the tendency to reproduce sexually, and with populations that are
limited in size. These recent efforts have clariFed the conditions that
are most likely to explain why sex is so common, as exempliFed by
the articles in this symposium issue of the
Sexual reproduction is a costly endeavor. In order to out-
cross, an individual has to Fnd a potential partner, attract
it, risk contracting sexually transmitted diseases, hazard
predation while mating (sometimes by the mate itself),
and forego opportunities to gather resources. ±or many
facultatively sexual species, there is an additional cost in-
volved in switching from mitotic to meiotic reproduction.
±or example, in
, mitotic replica-
tion occurs in
90 min, but the induction of meiosis takes
All of this effort would make sense if sex were a more
efFcient means of transmitting genes to future generations,
but it is not. A sexual parent transmits only 50% of its
genes to the next generation, compared with 100% for an
asexual parent. Thus, unless sexuals produce twice as many
offspring per individual, sexuality suffers from a trans-
mission disadvantage, a problem so acute that it has been
cost of sex (Bell 1982).
Last, but not least, sexual reproduction breaks apart
favorable combinations of genes built by past selection.
To hammer this point home, consider an analogy. Imagine
entering a poker hall after a game has been played. If you
were to offer the winners (holding, say, a 3
straight at one table, a three-queen hand Q
at another, etc.) the opportunity to keep
their hands or to shuf²e their cards with those of another,
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Am. Nat. 2009. Vol. 174, pp. S1–S14.
2009 by The University of Chicago.
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everybody would hold his or her cards. Winning hands—
those that have “survived” previous rounds—have cards
that work well with one another. Shuf²ing these cards
together produces descendant hands with no guarantee of
success (creating, e.g., a lousy hand of 3
). In all card games of interest, it is not enough to
know the suit and number of each card in isolation; rather,
the interactions among cards are what determine whether
the card is in a winning hand or a losing hand. Similarly,
genes do not work in isolation; the interactions among an