Abstract

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 (sensuKuhn, 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, 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 streamlined 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 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 frequently, 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.

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 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 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: “…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 long-lived, 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 pervasive 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) 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 effectiveness 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 sexually-reversed 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 non-heritable 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 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.

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

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

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.

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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