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Bateman (1948): Pioneer in the measurement of sexual selection

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NEWS AND COMMENTARY
Gems from the Heredity archive
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Bateman (1948): pioneer in the
measurement of sexual selection
MJ Wade and SM Shuster
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Heredity (2010) 105, 507–508; doi:10.1038/hdy.2010.8; published online 10
February 2010
Darwin (1871) identified sexual se-
lection as the process whereby the
members of one sex, generally
males, compete with one another for
reproductive access to members of the
other sex, generally females. He argued
that sexual selection should be a much
stronger evolutionary force in poly-
gamous than in monogamous mating
systems, and that, in the former, such
selection would fall primarily on mem-
bers of the male sex. Nearly 80 years
later, in his classic fruit fly study, Bate-
man (1948) reported the first empirical
demonstration that the cause of the sex
difference in intensity of selection was
variation among males in mate num-
bers. This seminal paper set the stage
for much of the modern research into
sexual selection.
Bateman’s stated goal was to identify
(p 352) ‘a fundamental cause of intra-
masculine selection, independent of
mating system and probably inherent
in the mechanics of sexual reproduc-
tion.’ He presumed that this cause
would reveal ‘why it is a general law
that the male is eager for any female,
without discrimination, whereas the
female chooses the male.’ Bateman
addressed the matter of sex differences
not in terms of behavior, as Darwin
did (with ‘arduous’ males and ‘coy’
females), but rather in terms of the
intensity of intra-sexual selection acting
within each sex. Bateman then inter-
preted his results in terms of sexual
differences in morphology, including
gamete size and tendencies to provide
parental care. Thus, Bateman’s contri-
bution simultaneously gave rise to the
two leading approaches to sexual selec-
tion and mating systems research that
exist today: (1) the conceptual and
empirical focus on sex differences in
parental investment (Williams, 1966;
Trivers, 1972; Emlen and Oring, 1977)
and (2) the theoretical and empirical
focus on measuring sexual selection itself
(Wade, 1979; Wade and Arnold, 1980;
Shuster and Wade, 2003; Jones, 2009).
In his experiments, Bateman estab-
lished 64 fly populations organized into
nine ‘series,’ each designed to explore
mating success and fitness for each sex
and to control for the effects of different
genetic markers, mating schedules, fe-
male life histories and genetic back-
grounds. Whereas modern sexual
selection researchers use microsatellites
to document paternity and maternity,
Bateman used a suite of visible single-
gene mutations to uniquely identify the
parents of each offspring in his popula-
tions. Although Bateman’s genetic mar-
kers did not have the advantage of
neutrality that microsatellites do, this
apparent constraint necessitated his
extraordinarily detailed set of experi-
mental controls, as well as the elegant
statistical methods used in analyzing his
results.
For example, to avoid inbreeding,
Bateman used different markers in
males and in females, guaranteeing that
all offspring from which matings per
parent were to be inferred would be
double heterozygotes, not homozygotes.
Bateman also emphasized that he was
measuring the actual fertility of indivi-
duals rather than their potential con-
tributions to the next generation. He
recognized how this limited his infer-
ences of the number of mating attempts:
‘the number of inseminations y
should, however, be regarded as a
minimum, for two reasons: the possibi-
lity that some matings might be ineffec-
tive, and the inability to distinguish
single and multiple inseminations in-
volving the same pair of flies.’ (p 353).
The same limitations apply to micro-
satellite estimates of parentage, but are
seldom as well recognized. Bateman
also noted that uncontrolled viability
differences among matings were more
likely to reduce rather than increase the
variance in offspring numbers within a
series, making his observed results
conservative.
Even with these constraints, Bate-
man’s results were consistent and
striking. He observed a sex difference
in the variance in fertility that was
greater for males than for females in
every series. Bateman also noted (Table 7;
p 360) ‘whereas only 4% of females
were unrepresented in progeny, 21% of
the males were unrepresented.’ Males
were five times more likely to fail in
reproductive competition than females.
Importantly, when Bateman subtracted
the sum of squares owing to the effect of
mate numbers from the total sums
of squares, he found the remainder to
be equal for the two sexes. He summar-
ized his findings in the often-repeated
quotation: ‘Variance in number of mates
is, therefore, the only important cause of
the sex difference in variance of ferti-
lity.’ These famous words were also
presented in his Figure 1 (p 362) as a
linear relationship between mate number
and offspring number for males and a
much smaller, but similar effect for
females. Such regressions today are com-
monplace and are referred to as ‘Bateman
Gradients’ (Arnold and Duvall, 1994),
consistent with Bateman’s observation
that ‘a sex difference in the variance in
fertility is therefore a measure of the sex
difference in intensity of selection.’
Several authors have claimed that
Bateman’s methods were flawed, inclu-
ding sampling problems that resulted
in unequal male and female mean
reproductive success, miscalculations
of variances, statistical pseudoreplica-
tion and selective presentation of data
(Snyder and Gowaty, 2007). These
authors imply that Bateman was
hindered in his conclusions by the
limitations of the markers he used, and
further that he was careless, even
dishonest, in how he conducted his
measurements and analyses. A careful
reading of Bateman (1948) reveals that
nothing could be further from the truth.
Bateman’s original emphasis was on
mean squares to capture the ‘gross
variability’ in fertility among males
and among females within each mating
series. In every case, even when reci-
procal matings were made between
males and females from different mar-
ker lineages, the variation in male
fertility was significantly greater than
for females. Far from an attempt to
inflate the degrees of freedom used in
his analysis, this approach accurately
measured the fitness variance for each
sex within each series, and his signifi-
cance tests of these variance ratios
showed the relationship he needed to
make his points.
Other authors (Sutherland, 1985;
Hubbell and Johnson, 1987) have sug-
gested that, because random mating can
lead to sex differences in mating suc-
cess, Bateman’s data do not show the
actual cause of sexual selection. This
Heredity (2010) 105,507–508
&
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criticism ignores Bateman’s partitioning
of the separate variance component for
mate numbers from the total variation
in fertility, as well as the internal
consistency of the results across series,
and the layers of controls he applied.
The authors, as well as other adherents
to the notion that chance is causal in
studies of sexual selection, neglect to
acknowledge that chance is part of any
study of selection. Some individuals
survive, mate and reproduce by chance,
whereas others do not, even if preferred
or favored attributes exist within the
population. This is why the probability
of fixation of a ‘good gene’ with positive
effect on fitness, s40, is only 2sinstead
of 1.0 (Kimura, 1962).
What makes Bateman’s results defini-
tive is that certain markers appeared
disproportionately among progeny, in-
dicating that some individuals mated
and others did not. This result led to the
most enduring conclusion of his work,
the signature cause of sexual selection:
the sex difference in fertility, which
causes the positive regression of off-
spring numbers (fertility) on mate num-
bers for males. Bateman distilled his
findings to a single statement that is as
powerful today as it was in 1948 (p 364):
‘Variance in number of mates is, there-
fore, the only important cause of the sex
difference in the variance in fertility.’
Conflict of interest
The authors declare no conflict of inter-
est.
Dr MJ Wade is at the Department of Biology,
Indiana University, 1001 East 3rd Street, Bloo-
mington, IN 47405, USA and Dr SM Shuster is at
the Department of Biological Sciences, Northern
Arizona University, Flagstaff, AZ 86011-5640,
USA.
e-mail: mjwade@indiana.edu
Arnold SJ, Duvall D (1994). Animal mating
systems: a synthesis based on selection theory.
Am Nat 143: 317–348.
Bateman AJ (1948). Intra-sexual selection in
Drosophila. Heredity 2: 349–368.
Darwin CR (1871). The Descent of Man and Selection
in Relation to Sex. Appleton: New York.
Emlen ST, Oring LW (1977). Ecology, sexual
selection, and the evolution of mating systems.
Science 197: 215–223.
Hubbell S, Johnson L (1987). Environmental
variance in lifetime mating success, mate
choice, and sexual selection. Am Nat 130:
91–112.
Jones AG (2009). On the opportunity for sexual
selection, the Bateman Gradient and the max-
imum intensity of sexual selection. Evolution
63: 1673–1684.
Kimura M (1962). On the probability of fixation
of mutant genes in a population. Genetics 47:
713–719.
Shuster S, Wade M (2003). Mating Systems and
Strategies. Princeton University Press: Princeton,
NJ.
Snyder BF, Gowaty PA (2007). A reappraisal of
Bateman’s classic study of intrasexual selec-
tion. Evolution 63: 2457–2468.
Sutherland WJ (1985). Measures of sexual selec-
tion. Oxford Surv Evol Biol 2: 90–101.
Trivers RL (1972). Parental investment and sexual
selection. In: Campbell B (ed). Sexual Selection
and the Descent of Man. Aldine Press: Chicago,
IL, pp 136–179.
Wade MJ (1979). Sexual selection and variance in
reproductive success. Am Nat 114: 742–764.
Wade MJ, Arnold SJ (1980). The intensity of sexual
selection in relation to male sexual behaviour,
female choice, and sperm precedence. Anim
Behav 28: 446–461.
Williams GC (1966). Adaptation and Natural Selec-
tion. Princeton University Press: Princeton, NJ.
Editor’s suggested reading
Johnston SE, Beraldi D, McRae AF, Pemberton JM,
Slate J (2010). Horn type and horn length genes
map to the same chromosomal region in Soay
sheep. Heredity 104: 196–205.
Dobler R, Hosken DJ (2010). Response to selection
and realized heritability of sperm length in
the yellow dung fly (Scathophaga stercoraria).
Heredity 104: 61–66.
News and Commentary
508
Heredity
... However, over the years, and especially after 2004, criticisms of the paper have amassed to the extent that biologists are now divided into two groups: those who praise Bateman as one of the founding fathers of the discipline of behavioural ecology (e.g. Wade & Shuster, 2010), and those who claim that Bateman's paper was empirically or theoretically flawed (e.g. Gowaty, Kim, & Anderson, 2012;Hrdy, 1986;Snyder & Gowaty, 2007;Sutherland, 1985), or that modern data do not support his paradigm (e.g. ...
... Hrdy; Gowaty; Altmann; Tang-Martínez), the early enthusiasts for Bateman's research do not have the slightest doubt about the validity and importance of his research. Sixty-two years after the original publication of Bateman's paper, the journal Heredity, in its section 'Gems from the Heredity archive', published a joint contribution by Wade and Shuster (2010) titled 'Bateman (1948): pioneer in the measurement of sexual selection'. This paper provides a good example of the rationale behind the persistent praise of Bateman's paper: Wade and Shuster (2010, p. 507) opine that Bateman's classic paper provides 'the first empirical demonstration that the cause of the sex difference in intensity of selection was variation among males in mate numbers'. ...
Article
In 1948, British geneticist A. J. Bateman published in the journal Heredity the results of his experiments on the fruit fly Drosophila melanogaster. Bateman hoped he was bringing evidence for the ‘greater dependence of males for their fertility on frequency of insemination’ (Bateman, 1948, Heredity, 2(3), p. 364), thus purportedly explaining ‘an undiscriminating eagerness in the males and a discriminating passivity in the females’ (p. 365). At first rather neglected, Bateman's results were increasingly cited in the 1970s, especially as Bateman had suggested that what he had discovered in Drosophila could also be applied to humans. However, throughout the years, criticisms of the paper accumulated to the point that biologists are now divided into two groups: those who praise Bateman as one of the founding fathers of the discipline of behavioural ecology, and those who claim his paper was fatally flawed. The present paper follows the ‘strange fate’ of Bateman's article: initially barely cited, the paper was ‘rediscovered’ by Robert Trivers in 1972 (Trivers, 1972, Parental investment and sexual selection. In B. G. Campbell (Ed.), Sexual selection and the descent of man: The Darwinian pivot, pp. 136–179, New Brunswick, NJ: Transaction Publishers) and finally, the paper received numerous scathing critiques in more recent years, on a methodological and empirical basis.
... Such strategies being an outcome of sexual selection primarily originate from reproductive asymmetries between the genders (Darwin 1871). The consequences of these asymmetries have been empirically demonstrated via the Bateman gradient (Bateman 1948), which although being widely debated (Arnold and Duvall 1994;Snyder and Gowaty 2007) still hints to crucial patterns underlying discrepancies between male and female reproductive success (Wade and Shuster 2010;Parker and Birkhead 2013). Due to constraints of gestation and parental care, females are biologically limited in the number of surviving offspring they can produce in their lifetime. ...
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In species exhibiting infanticide by males, females lose out with high stakes and should adopt pre-emptive mechanisms, pitching the genders in an evolutionary arms race for maximizing fitness. African lions remain a quintessential model of this gender war, with a coalition of males gaining temporary but exclusive breeding rights over a female-group after killing all cubs of former males. However in Asiatic lions, now found as a single population in Gir forests, India; adults live in same-sex groups that interact primarily for mating. Intensive monitoring of 70 adult lions revealed that female-groups (n=9) used exclusive territories while male ranges (n=11 coalitions) overlapped at areas of intense female use. A social-network of mating events (n=76) indicated that lionesses mated with multiple rival coalitions before conceiving. These neighboring coalitions, although hostile to each other were tolerant towards the same litters; suggestive of confused paternity amongst them. Given a land-tenure system where lionesses encounter many males capable of killing unfamiliar cubs, multi-male mating buffers cub infanticide and likely diversifies paternal lineages in litters. Consequently, infanticide was observed only when ‘new’ males invaded a female-group’s territory. An age-based mate-choice was observed in lionesses: maiden breeders chose males having highest range overlaps, while experienced females selected peripheral males. The inter-gender spacing patterns and resultant sexual strategies of lions differ in Asia and Africa probably because of contrasting resource availability, highlighting behavioral plasticity within species inhabiting diverse eco-regions. By mating with multiple males, lionesses safeguard their investments and outdo the males in the war of fitness.
... In contrast, when responders, with their fecundities reduced by contraceptives, also remain within the population in their pre-treatment proportions, non-responders, despite their apparent fitness advantage, represent only a tiny fraction of the total population. In a world where bad things can happen to good genes and vice versa, when non-responders are rare, their probability of increasing in frequency is surprisingly small, despite their seemingly large fitness advantage (Wade and Shuster, 2010). ...
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We illustrate a method for delaying and possibly eliminating the evolution of non-responsiveness to the treatments now used to control pest populations. Using simulations and estimates of the variance in relative fitness, i.e., the opportunity for selection, in a rat-like mammal, we show that the selection responsible for the evolution of non-responsiveness to pesticides and sterility-inducers, is similar in its action to sexual selection, and for this reason can be orders of magnitude stronger than that which exists for untreated populations. In contrast, we show that when contraceptives are used to reduce the fertility of a pest species, with non-responders embedded within such populations, the opportunity for selection favoring non-responsiveness is reduced to that which is expected by chance alone. In pest species with separate sexes, we show that efforts to control pest populations or to mitigate selection favoring non-responsiveness, are likely to be ineffective when members of one sex are sterilized or killed. We also show that while mating preferences can impede the rate at which resistance evolves, they are more likely to accelerate this process, arguing against the use of sterile male The opportunity for sexual selection and the evolution of non-responsiveness to pesticides, sterility inducers and contraceptives. approaches for controlling pests. Our results suggest that contraceptives are more effective at controlling pest populations and slowing the evolution of non-responsiveness than treatments that cause sterilization or death in target species. Furthermore, our results indicate that contraceptives that work differentially on each sex will be most effective in mitigating selection favoring non-responders. Our results have significant implications for the development and application of treatments to manage pests, now and into the future.
... Les diferències en forma i funció dels gàmetes són determinants per explicar els diferents rols de mascles i femelles en la reproducció: Bateman (1948) va poder demostrar experimentalment en la mosca del vinagre (Drosophila melanogaster) que els mascles tenien un èxit reproductor molt més variable entre individus que no pas les femelles i que els mascles podrien augmentar més ràpidament el seu èxit sexual simplement augmentant el nombre de còpules. Com a conseqüència, la competència per a l'accés a la reproducció és molt més intensa en els mascles, perquè s'hi juguen molt (Jones, 2009;Wade i Shuster, 2010). Bateman creia que aquestes diferències entre sexes es devien originalment en les asimetries en la inversió en els gàmetes. ...
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Després de culminar 20 anys de minuciós tre-ball d'investigació amb la publicació de l'"Origen de les espècies" (On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life, en anglès; Darwin, 1859), Charles Darwin no descansa. Està determinat a adreçar tots els aspectes criticats de la teoria i durant els següents anys es dedica a revisar notes, ampliar informació i corregir les edi-cions successives de l'"Origen". Hi ha un tema que té a Darwin especialment capficat: si els caràcters que se seleccionen són els que confereixen més probabilitat de supervivència, per què els mascles d'algunes espècies tenen colors atractius o cues extravagants que semblen anar en detriment de la supervivència dels individus? Cal trobar una ex-plicació. La selecció natural i la selecció sexual Uns mesos abans de la publicació de l'"Origen de les espècies", Charles Darwin i Alfred Russel Resum: La lluita per aconseguir reproduir-se és una part essencial de l'existència de qualsevol organis-me. Per als animals sexuats, l'afer es veu complicat per la necessitat de trobar un altre individu disposat a aparellar-se. Charles Darwin va ser el primer que va estudiar els sistemes d'aparellament des d'una òptica evolutiva i va posar la primera pedra de la teoria de la selecció sexual. Tot i que va caldre més d'un segle per convèncer els científics de la seva validesa, ha esdevingut una de les àrees més fecundes en el camp de la biologia evolutiva. Segons la teoria, els caràcters que confereixen als individus més possibilitats de deixar descendència, malgrat que puguin comprometre la seva supervivència, seran seleccionats per dos mecanismes diferents. Per una banda, els individus d'un mateix sexe competiran entre si per aconseguir aparellar-se amb l'altre sexe, de manera que se seleccionaran caràcters que els facin bons competidors. Per altra banda, els individus d'un sexe, generalment les femelles, podran elegir quin individu els fa més el pes per aparellar-s'hi, de manera que es podran seleccionar trets que per alguna raó fan els individus més atractius a ulls de l'altre sexe. Sota aquesta perspectiva, la teoria de la selecció sexual ha mirat d'explicar perquè són els mascles els que normalment lluiten i perquè les femelles les que majoritàriament són més exigents a l'hora d'escollir parella. A més, ha permès entendre una gran varietat de comportaments extra-vagants en el context del sexe: còpules furtives, amants transvestits, regals nupcials o suïcidis sexuals. Tot s'hi val en la lluita per la reproducció! Summary: Sexual Selection: why do maleS fight and femaleS chooSe?-The struggle to reproduce is a key part of the existence of any organism. For sexually reproductive species, reproduction is more difficult because they need to find another individual willing to mate. Charles Darwin was the first to study mating systems from an evolutionary point of view and he laid the first stone of sexual selection theory. More than one century was needed to convince the scientific community of its validity, but it has become one of the most active areas in the field of evolutionary biology. According to the theory, the traits that give individuals higher reproductive output, though they often compromise their survival, may be selected by two different mechanisms. First, individuals of the same sex compete with each other to copulate with the other sex, so any character that makes them good competitors should be selected. Second, the individuals of a given sex, usually the females, are able to choose which individual they prefer to mate with, so they can select attractive traits in the eyes of the other sex. From this perspective, sexual selection theory has explained why males usually fight and females are the choosy sex. In addition, it has increased understanding of a great variety of extravagant behaviours in the context of sex: furtive mating, cross-dressing lovers, nuptial gifts and sexual suicide. Everything counts in the struggle for reproduction!
... In addition, there are some species where sex differences in fitness do not depend principally on partner number in either sex [25]. However, the effects of partner number on female breeding success are typically small [26] and Bateman's fundamental insight that, where males do not care for their offspring, sex differences in the relationship between partner number and reproductive success ('Bateman gradients') commonly generate larger individual differences in breeding success, more frequent reproductive competition, more intense selection and a greater development of secondary sexual characters in males represents one of the cornerstones of modern evolutionary theory [6,7,27,28]. Bateman attributed the presence of sex differences in reproductive variance and Bateman gradients to sex differences in the size and rate of production of gametes and in the extent of parental care. ...
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This paper traces the development of our understanding of the development of different approaches to estimating the strength of reproductive competition and sexual selection in the two sexes, based on measures of the operational sex ratio, the opportunity for sexual selection and contrasts in selection gradients between the sexes. It argues that different approaches provide complementary insights into the causes of sex differences in reproductive competition, the operation of sexual selection and the evolution of secondary sexual characters and that improvements in our understanding of the evolution of secondary sexual characters will require a more comprehensive understanding of the ways in which social and ecological conditions modify reproductive competition and development in females and males. This article is part of the themed issue ‘Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies’.
... Proceedings of the National Academy of Sciences of the United States of America 106, 10009-10016. may contribute to selection, and may incorrectly assign evolutionary importance only to measured characters (Lande and Arnold, 1983;Wade and Shuster, 2010). Moreover, direct estimates of selection may overestimate the possible response to selection because they may detect significant covariance even when the total opportunity for selection is comparatively small (Hersh and Phillips, 2004). ...
Chapter
The utility of the operational sex ratio as an unqualified proxy for sexual selection intensity appears to be unfounded and the relationships between OSR and actual measures of sexual selection have proven inconsistent within and among species. Thus, estimates of OSR are not equivalent to those for sexual selection and are unlikely account for observed patterns of evolutionary change. Nevertheless, OSR is useful for characterizing experimental populations, and for manipulating competitive circumstances to observe behavior in particular species. Thus, the kinds of information obtained in past and present estimates of OSR and the spatial and temporal distributions of breeding adults can have evolutionary application, provided that the details of the experimental system and how changes in the level of competition among members of each sex are clearly known.
... Our use of the opportunity for selection also allows us to partition our empirical estimate of the maximum strength of selection into pre-copulatory and post-copulatory components, adding additional precision to our measures [2]. Such information is not available from direct estimates of the covariance between a particular phenotype and fitness [12]. Additional considerations for direct estimates of selection are reviewed elsewhere [5][6][7][8][9][10][11]. ...
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In 1948, Angus Bateman published a paper on fruit flies that tested Charles Darwin's ideas of sexual selection. Based on this one fruit fly study, Bateman concluded that because males are able to produce millions of small sperm, males are likely to behave promiscuously, mating with as many females as possible. On the other hand, because females produce relatively fewer, larger, and presumably more expensive eggs, females are likely to be very discriminating in selecting only one high-quality sexual partner. He also posited that a male's reproductive success increases linearly with the number of females he is able to mate with, but that a female's reproductive success peaks after she mates with only one male. Consequently, in almost all organisms, sexual selection acts most strongly on males. These ideas became a recurring theme in attempts to explain wide-ranging differences in male and female behavior not only in nonhuman animals but also in humans. As such, Bateman's conclusions and predictions have become axiomatic and, at times, have gone unquestioned even when modern empirical data do not conform to this model. This article reviews the origins and history of these ideas and uses modern data to highlight the current and growing controversy surrounding the validity and general applicability of this paradigm.
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This book presents the first unified conceptual and statistical framework for understanding the evolution of reproductive strategies. Using the concept of the opportunity for sexual selection, the authors illustrate how and why sexual selection, though restricted to one sex and opposed in the other, is one of the strongest and fastest of all evolutionary forces. They offer a statistical framework for studying mating system evolution and apply it to patterns of alternative mating strategies. In doing so, they provide a method for quantifying how the strength of sexual selection is affected by the ecological and life history processes that influence females' spatial and temporal clustering and reproductive schedules. Directly challenging verbal evolutionary models that attempt to explain reproductive behavior without quantitative reference to evolutionary genetics, this book establishes a more solid theoretical foundation for the field. Among the weaknesses the authors find in the existing data is the apparent ubiquity of condition-dependent mating tactics. They identify factors likely to contribute to the evolution of alternative mating strategies--which they argue are more common than generally believed--and illustrate how to measure the strength of selection acting on them. Lastly, they offer predictions on the covariation of mating systems and strategies, consider the underlying developmental biology behind male polyphenism, and propose directions for future research. Informed by genetics, this is a comprehensive and rigorous new approach to explaining mating systems and strategies that will influence a wide swath of evolutionary biology.
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Following principles used by A. J. Bateman, we identify the relationship between fecundity and mating success as the central feature in the operation of mating systems. Using selection theory from the field of quantitative genetics, we define the sexual selection gradient as the average slope of the relationship between fecundity and mating success and show how it can be estimated from data. We argue that sexual selection gradients are the key to understanding how the intensity of sexual selection is affected by mate provisioning, parental investment, and sex ratio.
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Analyzes the role of change, expressed in terms of the likelihood of survival and mate encounters, in mate-choice strategies and variances in lifetime mating success (LMS) for males and females. Using Markovian mating models, analytical expressions are derived for mean and variance for LMS as a function of the probabilities of survival and mate encounters per unit of time and of the duration of postmating latency, when individuals do not search for mates. If males have a similar survival rate but shorter postmating latencies than females, then males always exhibit higher variances in LMS than do females, given equal LMS means for both sexes. Simply observing a higher LMS variance for males than for females is not sufficient proof of the existence of sexual selection or male-male competition. Absolute LMS variances generally increase with increased survival, decreased duration of postmating latency, and increased mate availability. However, the ratio of male to female LMS variances first increases and then decreases with increasing survival; this ratio can become quite large if the length of postmating latency differs greatly between the sexes. Mate choice is favored by a sexual asymmetry in postmating latencies. Males generally have shorter postmating latencies than females; this implies that females should be choosier in their selection of mates at all levels of survival and of availability of potential mates. This is expressed by the smaller difference in potential mate quality required for female to be choosy. -from Authors
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In the current resurgence of interest in the biological basis of animal behavior and social organization, the ideas and questions pursued by Charles Darwin remain fresh and insightful. This is especially true of The Descent of Man and Selection in Relation to Sex, Darwin's second most important work. This edition is a facsimile reprint of the first printing of the first edition (1871), not previously available in paperback. The work is divided into two parts. Part One marshals behavioral and morphological evidence to argue that humans evolved from other animals. Darwin shoes that human mental and emotional capacities, far from making human beings unique, are evidence of an animal origin and evolutionary development. Part Two is an extended discussion of the differences between the sexes of many species and how they arose as a result of selection. Here Darwin lays the foundation for much contemporary research by arguing that many characteristics of animals have evolved not in response to the selective pressures exerted by their physical and biological environment, but rather to confer an advantage in sexual competition. These two themes are drawn together in two final chapters on the role of sexual selection in humans. In their Introduction, Professors Bonner and May discuss the place of The Descent in its own time and relation to current work in biology and other disciplines.