INTEGR. COMP. BIOL., 45:821–830 (2005)
The Problem with Paradigms: Bateman’s Worldview as a Case Study1
ZULEYMA TANG-MARTINEZ2
AND
T. BRANDT RYDER
Department of Biology, University of Missouri–St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121
SYNOPSIS.
Bateman’s principles, their corollaries and predictions constitute a paradigm for the study of
sexual selection theory, evolution of mating systems, parental investment theory, and sexual dimorphism in
male and female behavior. Some aspects of this paradigm have been challenged in recent years, while others
have been supported by empirical and theoretical research. We re-examine Bateman’s 1948 paper in detail,
including some methodological problems. Additionally, we review three areas in which an over-reliance on
Bateman’s predictions about sexual dynamics hindered our ability to understand the potential importance
of certain behaviors: 1) male mate choice and sperm allocation; 2) the role of females in initiating and
soliciting extra-pair copulations and fertilizations; and 3) the role of females in lekking systems, in which
recent evidence suggests that copulations with multiple males (polyandrous behavior) may be common. We
conclude this introduction to the symposium by emphasizing the heuristic value of Bateman’s contributions,
as well as the problems that arise when Bateman’s paradigm is viewed through the lens of modern behavioral
ecology and evolutionary theory.
INTRODUCTION
Paradigms in science (sensu Kuhn, 1970) can have
both positive and negative aspects. On the positive
side, paradigms serve as a framework that is understood and accepted by all workers in a field. As such,
paradigms provide a world-view that helps us to frame
questions and interpret results. In a sense, the paradigms act as a ‘‘lingua franca’’ that facilitates communication among scientists. On the negative side,
paradigms can lead to simplification, can blind us to
phenomena that do not fit the accepted world-view,
can guide us to accept hypotheses that are unfounded,
and can prevent us from considering alternative hypotheses and explanations. In such cases paradigms
become dogma and have detrimental effects on the development of scientific ideas.
We consider the ideas presented by Bateman (1948;
all further citations of Bateman refer to his 1948 paper), and the subsequent elaboration of his ideas (e.g.,
by Williams, 1966; Trivers, 1972; Wilson, 1975; Parker, 1979), as a ‘‘paradigm’’ in behavioral ecology. It
provides the fundamental underpinnings for much of
the research that focuses on sexual behavior, sexual
selection, parental care, and evolution of mating systems.
Bateman’s research on fruit flies (Drosophila melanogaster) examined ideas on sexual selection and
male-female differences in sexual behavior originally
proposed by Darwin (1871). At a time when molecular
techniques were not available, Bateman’s experiments
were ingenious and elegant, although in retrospect we
can find fault with some aspects of his experimental
design. His basic conclusions were that ‘‘the sex difference in variance of fertility . . . is due to the effect
of number of mates per fly on fertility’’ and that ‘‘the
stronger correlation, in males, between number of
mates and fertility . . . is the cause of intra-masculine
selection’’; consequently, ‘‘sexual selection is much
more effective in males than in females’’ and ‘‘variance in fertility is in fact a measure of (sexual) selection’’ (Bateman, pp. 362–363 and 353). Bateman’s
conclusion have, in modern times, been elaborated into
three postulates or ‘‘principles’’: a) male reproductive
success (RS) increases as a function of the number of
females with which a male mates, but mating with
more than one male should not increase a female’s RS;
b) male RS shows greater variance than female RS;
and c) the sex with the greater variance in RS (typically males) should be the more sexually-selected sex.
These postulates, particularly those relating variance
in RS to the strength of sexual selection, have been
widely accepted and are extremely influential (e.g.,
Wade, 1979; Arnold, 1994; Arnold and Duvall, 1994;
Jones et al., 2002).
In this paper we refer to the whole of Bateman’s
ideas (including postulates, premises, predictions, and
elaborations) as Bateman’s paradigm; however, occasionally we use the term ‘‘principle’’ when referring
to the work of other investigators who focused more
narrowly on one or more of the postulates discussed
above. We concentrate on the entirety of Bateman’s
thesis, because we believe that a thorough examination
of the role that Bateman has played in behavioral ecology requires an understanding of the premises on
which his ideas are based and the behavioral predictions that follow from them.
Bateman’s postulates rest on the premise of anisogamy: that males can produce unlimited numbers of
small sperm, while females produce only a limited
number of large eggs. Therefore, he reasoned, males
should be sexually indiscriminate and promiscuous,
mating with as many females as possible; females, on
the other hand, should be coy, sexually passive, and
very choosy, mating only with the ‘‘best male’’ who,
1 From the Symposium Bateman’s Principle: Is It Time for a Reevaluation? presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5–9 January 2004, at New Orleans, Louisiana.
2 E-mail: zuleyma@umsl.edu
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because of his prodigious production of sperm, should
be able to fertilize all her eggs. In his view, the primary cause of sexual selection is ‘‘that females produce much fewer gametes than males’’ (Bateman, pp.
364–365). Bateman attributed greater variance in male
RS and males’ greater responsivity to sexual selection
to sexual differences in behavior: coy, choosy females
and indiscriminate males. Thus, he (p. 365) predicted
that anisogamy would ultimately result in ‘‘an undiscriminatory eagerness in the males and a discriminatory passivity in the females,’’ and that ‘‘greater dependence of males for their fertility on frequency of
inseminations’’ is ‘‘an almost universal attribute of
sexual reproduction’’ (p. 364).
Bateman implies that sperm are less expensive to
produce than eggs, but does not state so explicitly.
Subsequent papers that rely on Bateman’s ideas are
explicit when they posit that eggs require large energy
expenditure or investment, while sperm do not (e.g.,
Williams, 1966; Orians, 1969; Trivers, 1972; Wilson,
1975; Parker, 1979).
We contend that an over-reliance on some of Bateman’s views, particularly those related to the importance of anisogamy and differences in sexual behavior
of males and females, has led to unquestioned assumptions that may not always be correct. Additionally, important theoretical critiques of Bateman have,
at times, been neglected (e.g., Sutherland, 1985; Hubbell and Johnson, 1987; but see Arnold and Duvall,
1994; Gowaty and Hubbell, 2005). This symposium
was motivated by the fact that modern data on male–
female sexual behaviors, and on differences between
the sexes in costs of reproduction, do not always accord with the predictions made by Bateman and later
advanced by Trivers (1972) and others (e.g., Williams,
1966; Dawkins, 1976; Parker, 1979). Moreover, while
the relationship between heritable variances in RS and
strength of sexual selection remains unquestioned,
some researchers (e.g., Hubbell and Johnson, 1987;
Gowaty, 2004) caution that random, non-heritable factors can also affect variance in RS without a concomitant impact on sexual selection. Finally, the assumption that females will invariably show lower variances
in RS and no increase in fertility as a function of the
number of mates is no longer tenable (e.g., Lanctot et
al., 1997; Worden and Parker, 2001; Lewis et al.,
2004; Levitan, 2005; Parker and Tang-Martinez,
2005).
In this introduction to the symposium, we suggest
that uncritical acceptance of Bateman’s paradigm has
led to, at least, two specific problems: a) simplification
of Bateman’s data, resulting in an incomplete and biased understanding of his original findings; and b) our
ability to interpret reality with regards to male and
female sexual behavior has been compromised.
SIMPLIFICATION
Dewsbury (1998) defines three types of scientific
simplification. In primary simplification the author of
a study condenses a large body of data into stream-
AND
T. B. RYDER
lined conclusions that make the paper more comprehensible to other scientists. Although this happens in
all reports of empirical research, usually in the ‘‘discussion’’ section of papers, this necessary condensation may emphasize some aspects of the work over
others, thereby contributing to possible later misinterpretations. In secondary simplification the same process continues in a more exaggerated form when the
same author publishes other papers. In tertiary simplification, scientists other than the author of the original
paper, cite the original work incompletely, dogmatically, or without acknowledging its limitations (e.g.,
in new papers, textbooks, or reviews); important aspects of the original data are overlooked and what is
cited tends to be narrowly focused.
Bateman’s work suffered from both primary and tertiary simplification (Bateman published only one paper
on this topic, so secondary simplification is not an issue). To understand the role that simplification played
in dogmatizing Bateman’s ideas, we provide a detailed
analysis of his experiments.
Bateman conducted six ‘‘series’’ of experiments and
analyzed them as two different sets that yielded different results, summarized in two graphs (Bateman’s
Figs. 1a and 1b, p. 362). The different series varied in
ways that could have influenced the results independently of male promiscuity or female choosiness. His
experiments consisted of placing several mutant flies
in a bottle and allowing them to mate ad lib. However,
the various series differed with regards to number of
flies per bottle, age of flies, duration of experiments,
number of days females were allowed to lay eggs, mutations used, pedigrees of parents, and levels of inbreeding (Bateman, Table 3). Bateman did not systematically observe the flies’ behavior; rather, he inferred
matings from the genetic markers (visible mutations)
carried by the progeny. Thus, he based his conclusions
only on inseminations that produced viable young
whose parents were ‘‘identifiable’’ (Bateman, p. 355
discusses problems encountered in identifying the parents of all offspring). Levels of inbreeding may have
affected fertility (Bateman, p. 355).
Bateman’s critical data are presented in two graphs
(p. 362; Fig. 1 this paper). Graph 1a shows the results
of series 1–4; graph 1b, those of series 5–6. The latter
graph is the only one that shows female fertility peaking after one mating. In contrast, Figure 1a shows that
both male and female fertility increases as a result of
siring young with more than one mate, although the
slope for males is greater. Bateman emphasized the
results in Figure 1b. Without ever monitoring behavior,
he concluded that these results were due to ardent,
indiscriminate males and passive, choosy females.
Primary simplification also is evident in Bateman’s
use of ‘‘mate’’ because, for a female, ‘‘number of
mates’’ really meant the number of males that sired
her young. Much of the subsequent literature has perpetuated this error by assuming that ‘‘mating success’’
is equivalent to ‘‘number of mates’’ as used by Bateman. In reality, Bateman had no way of knowing how
BATEMAN’S PARADIGM
AS A
CASE STUDY
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FIG. 1. Bateman’s two graphs showing relationship between number of mates and fertility for males and females. See Discussion in text.
(Redrawn from Bateman’s (1948, p. 362)) original graphs.
many times a female mated, or with how many males,
because he did not conduct behavioral observations
(Dewsbury, 2005).
Tertiary simplification has been critical in the dogmatization of Bateman’s paradigm. Trivers (1972),
Wilson (1975), Daly and Wilson (1983) and a number
of textbook authors (e.g., Alcock, 1989; Drickamer et
al., 2002; Krebs and Davies, 1993) present the data
from Figure 1b to illustrate Bateman’s Principle, while
ignoring Figure 1a. Thus, only one portion of Bateman’s experiments has been used to formulate one of
his best known ‘‘principles’’: that male RS increases
with number of mates, while female RS peaks after
mating with only one male. Moreover, in some cases,
Bateman’s data and methodology have been misrepresented and embellished when doing so strengthened
preconceived notions of male and female behavior
(Dewsbury, 2005).
Aspects of Bateman’s experimental design raise
questions. Birkhead (2000) suggests that flies in series
1–4 may have been food-limited, thereby biasing the
results. He may be referring to the fact that, in series
1–4, Bateman left the flies in the same bottle throughout the duration of the experiment (3 or 4 days), while
in series 5, he transferred flies to a new bottle every
day. Since Bateman gave no information on amount
of media used, it is impossible to determine if food
limitation occurred. However, Gowaty (personal communication) indicates that larval competition can vary
with the quality of the media, which can change over
time; if so, differential survival of identifiable offspring as a result of larval competition could have affected the results. Bateman’s use of D. melanogaster
also is controversial because females of this species
can store and use sperm for up to 4 days (Bateman’s
experiments lasted 3 or 4 days). Since in other Drosophila species, females need to copulate more fre-
quently, Birkhead (2000, p. 198) concludes: ‘‘Had
Bateman chosen a species that typically recopulates
more than every 3 or 4 days, Trivers would not have
been able to disregard those results which did not fit
his preconceptions about sexually motivated males and
reluctant females.’’
In a similar vein, Gowaty (1997a, 2003, 2004) suggests that females may have mated with fewer males
because D. melanogaster males produce seminal proteins that can increase females’ latencies to re-mate by
inhibiting receptivity. Thus, female ‘‘coyness’’ is induced by males rather than being an inherent characteristic of females. If receptivity was inhibited, the
very small sample sizes used by Bateman (3 or 5 flies
of each sex per experiment) may have effectively lowered the number of receptive females available, causing males to mate indiscriminately with any receptive
female they encountered. The age of the flies also may
have influenced the results because survival probabilities may affect male and female sexual behavior
(Hubbell and Johnson, 1987; Gowaty, 2004).
In summary, simplification occurred on the part of
Bateman, and of those who later popularized his ideas.
Ironically, the greater portion of Bateman’s data, presented in the largely forgotten Figure 1a, does not support the usual interpretations of Bateman’s findings because females also increase fertility with increasing
number of ‘‘mates.’’ Furthermore, Bateman’s tables 7
(p. 360) and 8 (p. 361) show that, while a larger proportion of males, as compared to females, failed to
produce progeny (i.e., males had greater variance in
RS), it is also true that most females produced progeny
(‘‘mated’’) with more than one male and that in most
of the experiments their fertility increased with the
number of sires. Without simplification it is unlikely
that Bateman’s research would have had the paradigmatic impact that it has enjoyed.
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Z. TANG-MARTINEZ
PREDICTIONS ABOUT MALE AND
FEMALE SEXUAL BEHAVIOR
Among Bateman’s most important popularizers is
Trivers (1972), whose influential paper on parental investment perpetuated the stereotypes of indiscriminate
males and sexually restrained females. Trivers (1972)
assumes that male and female parental and sexual behaviors can be explained by anisogamy and that females always start with a greater investment because
eggs are costly but sperm are cheap. At any point in
time, females will have invested more than males; consequently, females will safeguard their past investment
by continuing to invest in parental care, while males
will benefit by deserting their partner to seek additional mates. Thus, females will be predisposed to take
care of the young and remain monogamous, while selection will favor promiscuous males. Only under unusual circumstances will males invest more and females become sexually competitive and more subject
to sexual selection.
Although Gowaty (2003) points out that data from
diverse taxa fail to support several of Trivers’ (1972)
critical predictions, for many years the Bateman–Trivers perspective about female choosiness and male promiscuity was widely accepted. This acceptance hindered our understanding of: a) the costs of sperm production and the importance of male mate choice (because of space limitations we do not address other
male reproductive costs that also favor male mate
choice: territory defense, male–male combat, searching for females, increased risk of predation, and costs
of adornments); b) the role of females in actively soliciting sexual encounters, including extra-pair copulations and fertilizations; and c) lek dynamics and the
behaviors of females at leks. Although there are other
criticisms of Bateman’s work, we limit our discussion
below to these three topics.
Male choice and sperm limitation
As long as males were assumed to produce unlimited numbers of inexpensive sperm, the possibility of
sperm depletion and male mate choice were largely
ignored. Dewsbury (1982) was among the first to point
out the fallacy of comparing the cost of one egg to the
cost of one sperm: an ejaculate, consisting of millions
of sperm and accessory gland secretions, is necessary
to fertilize even one egg. He also emphasized that ejaculate cost and sperm competition could result in male
mate choice (Dewsbury, 1982).
Sperm costs, competition, and allocation are now
major areas of research (e.g., Birkhead and Moller,
1998; Simmons, 2001; Schaus and Sakaluk, 2001;
Wedell et al., 2002). In some species, sperm may be
a limited resource; females may be sperm-limited and
have lower RS because they mate with males that have
run out of sperm (Royer and McNeil, 1993; Warner et
al., 1995; Jones, 2001; Saether et al., 2001; Wedell et
al., 2002). In the context of Bateman, this is critical
AND
T. B. RYDER
because it can lead to increased variance in female
reproductive success.
Jaffe (2004) stresses that the production of large
numbers of sperm makes ejaculates costly but is likely
maintained because, by allowing gamete selection, it
favors sexual reproduction. Several examples illustrate
that sperm production carries significant costs. Production of sperm, rather than oogenesis, or the physical act of mating, reduces lifespan in Caenorhabditis
elegans, leading Van Voorhies (1992, p. 456) to state
that this finding ‘‘contradicts the traditional biological
assumption that large oocytes are much costlier to produce than small sperm.’’ Males of the marsupial
‘‘mouse,’’ Antechinus stuartii, produce only a small
quantity of sperm and the cauda epididymis limits the
number of sperm available during each ejaculation
(Taggart and Temple-Smith, 1990). After a brief period
of ‘‘mating madness,’’ during which they attempt to
mate with many females, males run out of sperm and
die (Renfree, 1992). Male adders (Vipera berus) lose
mass while immobile and building up sperm supplies.
The rate of mass loss is as high as when males are
active and engaging in reproductive behavior; Olsson
et al. (1997, p. 457) conclude that ‘‘sperm production
may be a more expensive component of reproduction
than has heretofore been assumed. . . .’’ Physiological
mechanisms responsible for the high costs of sperm
production are not fully understood.
Contrary to Dawkins’ (1976, p. 176) statement that
‘‘the word excess has no meaning for a male,’’ the
antiquated notion that males can produce virtually unlimited numbers of sperm at little cost is demonstrably
incorrect. Sperm depletion, as a result of previous ejaculations, has been reported in diverse invertebrate and
vertebrate taxa (e.g., Kaufmann and Demerec, 1942;
Freund, 1963; Halliday and Houston, 1978; Rutowski,
1979; Nakatsuru and Kramer, 1982; Dewsbury and
Sawrey, 1984; Birkhead and Fletcher, 1995; Gomez
and Serra, 1996).
Male responses to sperm depletion are variable. In
some species, males continue to copulate whether or
not they are capable of inseminating females (Lefevre
and Jonsson, 1962; Nakatsuru and Kramer, 1982;
Dewsbury and Sawrey, 1984); in others, males strategically allocate sperm to certain females (see below),
or stop mating when they no longer have enough
sperm to inseminate females (e.g., Halliday and Houston, 1978; Rutowsky, 1979; Adams and Singh, 1981;
Dewsbury and Sawrey, 1984). Despite these differences, males of all species appear limited in the numbers
of sperm they can produce and are subject to sperm
depletion (Dewsbury and Sawrey, 1984). The variation
in fertility and behavior of sperm-depleted males merits further study.
Sperm depletion should favor male mate choice, including sperm allocation. Males may allocate sperm
based on a female’s mating status (mated vs. unmated),
social rank, age, size, or health condition (Wedell et
al., 2002). In situations favoring sperm competition,
males may allocate more or less sperm per ejaculate
BATEMAN’S PARADIGM
depending on presence and number of rivals, and on
probability of encountering additional receptive females. In some species, males are so choosy that they
may simply refuse to mate when solicited by certain
females. Male European starlings (Sturnus vulgaris)
refuse 26% of female solicitations (Pinxten and Eens,
1997) and dominant, male great snipe (Gallinago media) frequently refuse to mate with the same female
more than once, and may even chase away soliciting
females (Saether et al., 2001). Likewise, in several
Drosophila species, some males are so choosy that
they avoid mating with certain females (Gowaty et al.,
2002, 2003a). Moreover, male mate choice may affect
subsequent male RS (e.g., Drickamer et al., 2003; Gowaty et al., 2003b).
The assumption that sperm production was unlimited was so widely accepted that pioneering papers emphasizing the potential importance of male mate choice
(e.g., Dewsbury, 1982; Dewsbury and Sawrey, 1984;
Johnson and Hubbell, 1984) were largely ignored.
Only recently has male choice become a preeminent
area of study (e.g., Gomez and Serra, 1996; Arnaud
and Haubruge, 1999; Hunter et al., 2000; Saether et
al., 2001; Gowaty et al., 2002, 2003a, b; Drickamer
et al., 2003; review by Wedell et al., 2002).
Female solicitation and extra-pair copulations
The revolutionary discovery that sperm from different males can compete in the reproductive tract of
one female (Parker et al., 1972) implicitly revealed
that females must be mating with multiple males. Multiple matings by females raise the possibility that females can select among sperm from different males, a
type of female choice that takes place in the female’s
reproductive tract (Birkhead and Moller, 1993; Eberhard, 1996). Interestingly, although they had observed
females mating with several males, Parker et al. (1972)
and Parker (1979) continued to assume stereotypical
male–female differences in sexual behavior. Thus,
while they understood the significance of sperm competition as a male reproductive strategy, they largely
failed to recognize the equally interesting and revolutionary implications of their findings for females (but
see Simmons, 1987).
The last thirty-five years have seen an abundance of
studies confirming that females in many species (e.g.,
primates: Goodall, 1971; Hrdy, 1977, 1986, 1997;
Snowdon, 1997; Parish and de Waal, 2000; Drea and
Wallen, 2003; felids: Eaton, 1978; birds: Parker and
Burley, 1998; references below; fruitflies: Gowaty et
al., 2002, 2003a) are sexually assertive, actively seek
multiple copulations, and routinely mate with more
than one male. Polyandry has been reported in other
social and non-social insects (e.g., Taber and Wendel,
1958; Tregenza and Wedell, 1998; Lewis et al., 2004),
arachnids (Newcomer et al., 1999), reptiles (Madsen
et al., 1992; Olsson et al., 1994), and mammals (e.g.,
Moller and Birkhead, 1989; Keil and Sachser, 1998).
In fact, females mating with multiple males is so prevalent that Newcomer et al. (1999, p. 10236) conclude:
AS A
CASE STUDY
825
‘‘. . . it is becoming clear that polyandry is a common
female mating strategy, although it is often covert and
difficult to detect at the behavioral level.’’
In the remainder of this section we concentrate on
birds, the taxon in which extra-pair copulations (EPCs)
and fertilizations (EPFs), have been studied most extensively. Over 85% of bird species are considered socially monogamous. Yet, of the socially monogamous
passerines in which paternity has been determined using molecular techniques, 75–85% were found to engage in EPFs, and true genetic monogamy occurred in
less than 7% of species (Bennet and Owens, 2002).
Rates of EPFs and extra-pair paternity (EPP) are
quite variable but can be very high. In the reed bunting
(Emberiza schoeniculus), 50% of offspring are extra
pair young (EPY) and 70% of clutches contain EPY
(Dixon et al., 1994). In the socially monogamous, but
cooperatively breeding, superb fairy wren (Malurus
cyaneus) 95% of clutches have EPY and 75% of
chicks are EPY (Mulder et al., 1994). More than 60%
of all attempted copulations in waved albatrosses
(Phoebastria irrorata) were with extra-pair males and
one female was observed to mate 81 times with 50
different males during one breeding season; 17% of
broods consisted of EPY (Huyvaert, 2004). These findings are surprising because waved albatrosses are longlived, socially monogamous procellariiforms whose
life history traits do not predict high levels of EPCs
or EPFs (Bennet and Owens, 2002; Huyvaert, 2004).
Early reports of EPCs and EPFs in birds (e.g., Marler, 1956; Bray et al., 1975; Gowaty and Karlin, 1984;
Gowaty, 1985) often were disregarded or misinterpreted. The stereotype of sexually restrained, highly
discriminating females did not provide a theoretical
framework that could make sense of these reports unless males were forcing unwilling females to mate. A
common assumption was that EPCs were initiated by
males intruding into neighboring territories and that
females passively and reluctantly acquiesced to males’
sexual advances. EPCs and EPFs were regarded as
male reproductive strategies that were probably detrimental to females (reviews by Gowaty, 1985; Stamps,
1997; Lawton et al., 1997).
It is now widely recognized that females in many
birds have significant control over EPCs and EPFs
(e.g., Gowaty, 1985, 1997b; Smith, 1988; Gowaty and
Bridges, 1991; Sheldon, 1994; Gray, 1997; Neudorf et
al., 1997); they initiate sexual interactions, actively solicit copulations from some males, and successfully
reject copulations from others. Even after mating, females may influence which sperm fertilize their eggs
by ejecting unwanted sperm or through physiological
mechanisms, including immunological responses,
chemical interactions in the reproductive tract, or preferential capacitation of sperm from different males
(Birkhead and Moller, 1993; Gomendio and Roldan,
1993). Furthermore, female RS may increase as a result of EPCs and EPFs (Griffith et al., 2002).
In summary, we agree with Newcomer et al.’s
(1999, pp. 10236) assertion that: ‘‘Polyandry as a per-
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Z. TANG-MARTINEZ
vasive feature of natural populations challenges the
long-held view of females as the choosy, monogamous
sex . . . ,’’ and with Birkhead’s (2000, p. ix) statement
that: ‘‘Generations of reproductive biologists assumed
females to be sexually monogamous but it is now clear
that this is wrong.’’
Polyandrous females at leks
The recent emphasis on female behavior led to the
discovery that, at least in some avian lekking species,
females mate polyandrously. The traditional view of
leks had been that males establish a display arena in
which they compete for females; females visit the lek
and chose the ‘‘best’’ male to mate with. In some species, the dominant male in the lek was reported to
obtain almost all the copulations and only a small proportion of males in a lek ever mated. Thus, leks represented extreme cases of male promiscuity in which
male variance in RS was enormous and female variance was virtually non-existent. There were two problems with this scenario: a) because of the assumption
that females are choosy and only need to mate with
one male, female behavior was rarely the focus of
studies at leks—in most cases we assumed what females were doing, but did not monitor their behavior
in detail; b) prior to the advent of molecular techniques
for determining paternity, we relied only on behavioral
observations which did not always reflect genetic reality.
This view of leks suffered a rude awakening when
Petrie et al. (1992) reported that female peahens (Pavo
cristatus) mate with several males in a lek and with
the same male more than once. Moreover, females aggressively defend their preferred males and repeatedly
solicit copulations. Since molecular techniques were
not used in this study, we know nothing about actual
paternity. However, the behavioral data are consistent
with sperm depletion and suggest that variance in female RS might be considerable.
Even more surprising were results of behavioral and
molecular studies conducted by Lanctot et al. (1997)
on buff-breasted sandpipers (Tryngites subroficollis).
Behavioral observations at several leks, during two
breeding seasons, were unremarkable. Female visits,
solicitations, and copulations were highly skewed. For
example, in one representative lek, one male was responsible for 80% of observed copulations in 1993 (a
second male for the remaining 20%), and for 100% in
1994. The majority of males at the leks were never
seen mating. However, DNA paternity analyses revealed that a minimum of 39 and 20 males had sired
offspring in the two years respectively, and more than
40% of broods were multiply sired. Most males were
represented in only one family, and only four males
sired more than four young. Thus, the genetic studies
found much lower variance in male RS than expected
from the behavioral data. Since most males sired only
one brood and many clutches were fertilized by multiple males both on and off leks, Lanctot et al. (1997)
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T. B. RYDER
concluded that, genetically, most males were monogamous, while most females were polyandrous.
Female sage grouse (Centrocercus urophasianus)
sometimes also mate with multiple males. However,
DNA analysis found that only 2 of 10 broods were
multiply sired and behavioral data were consistent with
the genetic results (Semple et al., 2001).
The ruff, Philomachus pugnax, has the highest rate
of polyandry in a lekking species (Lank et al., 2002).
Females routinely engage in multiple copulations with
more than one male, within and among leks; they also
solicit and copulate with satellite males. Genetic studies found that, at a minimum, 59% of clutches were
sired by more than one male, and some clutches contained young sired by three different males.
Although the aforementioned species may be anomalous, another possibility is that polyandrous matings
by females of lekking species may be more common
than has been assumed (reviewed in Lanctot et al.,
1997). Females copulate with multiple males in several
other species, but DNA paternity analyses are not
available. Females of numerous other species are
known to visit leks more than once and to mate off
leks, behaviors that may be associated with polyandrous matings.
CONCLUSION
We have used Bateman’s ideas to demonstrate some
of the pitfalls that can occur when a paradigm becomes
so embedded in scientific thinking that it is rarely
questioned. Although we do not deny that there are
differences in male and female behavior, we used
male–mate choice and active sexual behavior by females to illustrate how relying too heavily on Bateman’s predictions hindered our ability to understand
sexual dynamics.
Bateman’s assumption that sexually dimorphic patterns in variance in RS are due to sexually passive,
choosy females, and indiscriminate males, is problematic. Moreover, the notion that female RS reaches a
peak after only one mating is no longer tenable. In
numerous species, females that mate with multiple
males have higher RS than monogamous females (e.g.,
Madsen et al., 1992; Olsson et al., 1994; Keil and
Sachser, 1998; Ketterson et al., 1998; Newcomer et
al., 1999; Tregenza and Wedell, 1998; Worden and
Parker, 2001; Lewis et al., 2004).
Despite the influence of Bateman’s ideas, a paradigm shift is already well underway with regards to
male–female sexual dynamics (Gowaty, 1994). We
now know that females have evolved a variety of
mechanisms that allow them to exert control over their
own reproduction: they solicit EPCs, engage in cryptic
and indirect female choice (e.g., Eberhard, 1996; Wiley and Poston, 1996), instigate sperm competition by
mating with multiple males, and may choose preferred
sperm to fertilize their eggs (e.g., Simmons, 1987; Olsson et al., 1996). Female control also may involve
mechanisms by which they resist coercion attempts by
males; if it affects their RS, variance in the effective-
BATEMAN’S PARADIGM
ness of these resistance mechanisms can lead to strong
sexual selection in females (Gowaty and Buschhaus,
1998; Gowaty, 2004). As a result of this new view of
females, the study of conflict between the sexes and
its possible effects on sexual selection (Smuts and
Smuts, 1993; Gowaty, 1997a, 2004; Stockley, 1997)
have received increasing attention. On the other hand,
forms of cooperation between males and females may
influence RS in both sexes and should not be ignored
(Eberhard, 1996; Snowdon, 1997; Tang-Martinez,
2000). For example, in some insects, spermatophore
proteins, or other nuptial gifts, are used by females in
the production of eggs (e.g., Lewis et al., 2004). Cooperation also may be behavioral, as when female primates assist males during copulations (Kanawaga et
al., 1972), or may involve complex egg–sperm interactions (reviewed in Pitnick and Karr, 1996).
There is no question that Bateman’s contributions
have stimulated important empirical and theoretical research. Bateman’s basic theoretical insight relating
mating success to RS, and predicting that the sex
which has greater variance in RS will be the sex that
experiences stronger sexual selection, is undeniably
correct. The reversal of Bateman gradients in sexuallyreversed species can be interpreted as additional, support for Bateman’s principles (e.g., Jones et al., 2002;
Jones et al., 2005). Yet, even here, a caveat is offered
by Gowaty (2004, p. 42): ‘‘. . . to demonstrate sexual
selection it is not enough to show that there are variance differences between or among the sexes, because
some variance differences necessarily arise due to nonheritable environmental forces’’; to show sexual selection is at work, one must subtract the variance due to
non-heritable forces from those due to selection.
Bateman’s contributions also are relevant to mating
systems. In Bateman’s world view, males would naturally tend to be promiscuous, while females would
tend to be monogamous. When Trivers (1972) crafted
his parental investment theory, he concurred with these
predictions and made mating systems dependent primarily on past parental investment which, because of
anisogamy, was assumed to always be initially greater
in females.
We suggest that traditional views emphasizing male
promiscuity, female sexual passivity, and greatly differing costs of male and female reproduction do not
provide the best framework for understanding mating
system evolution and sexual selection. An alternative
approach is to take into account ecological, social, and
phylogenetic variables and constraints. In favoring this
approach we endorse the views of others (e.g., Emlen
and Oring, 1977; Hubbell and Johnson, 1987; Ligon,
1999; Wink and Dyrez, 1999; Bennet and Owens,
2002; Shuster and Wade, 2003; and Gowaty, 2004)
who emphasize the importance of environmental, social, and ecological variables, albeit not to the exclusion of other factors. However, even some of these
authors (e.g., Emlen and Oring, 1977; Shuster and
Wade, 2003) tend to address mating systems from a
AS A
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827
male-centered perspective that has become increasingly problematic.
This symposium examines the current state of
knowledge on various aspects of Bateman’s paradigm,
with a special emphasis on male–female sexual behavior, Bateman gradients, sexual selection, and evolution
of mating systems. Some papers disagree with our perspective, while others agree. Although some recent
findings do not support Bateman’s ideas, or offer only
equivocal support (e.g., Parker and Tang-Martinez;
Levitan; Leonard; Drea; Gowaty and Hubbell), other
data do provide strong empirical and theoretical support for important aspects of Bateman’s predictions
(e.g., Andrade; Jones et al.; Lorch). The papers that
follow present a range of positions based on studies
of diverse taxa with different life histories, ecologies,
and social systems. It is our hope that this symposium
will lead to serious and open inquiry about Bateman’s
paradigm. By refining our understanding of Bateman’s
work and considering diverse factors that can influence
Bateman’s predictions, the papers comprising this
symposium should bring us closer to consensus and
guide critical questions in the fields of animal behavior
and behavioral ecology.
ACKNOWLEDGMENTS
ZTM: I dedicate this paper to the memory of my
mother, Rosita Martinez de Tang, who died unexpectedly on 26 February 2004, in Caracas, Venezuela. I
will forever be grateful for her steadfast support of my
career and interest in my work. Despite little formal
education, her ingenuous opinions, including those
about Bateman, were always insightful, on target, and
often very witty.
I thank Don Dewsbury for suggesting this symposium; George Taylor, Jorge Luis Hurtado, and Nancy
Solomon for supplying references; Patty Gowaty for
reading the MS and providing invaluable comments
and references. The National Science Foundation generously funded the symposium (IBN-0343067). Both
authors jointly thank the members of the UMSL Animal Behavior Discussion Group for interesting discussions and valuable insights.
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