Category Archives: Journal Pub

Fritzsche & Arnqvist 2013: Homage to Bateman: sex roles predict sex differences in sexual selection

(NB: In spite of the authorship flag above, the section below is Claudia’s work, not mine! I am posting it on her behalf because she’s off somewhere sunny scuba diving, I think…. Luc)

I am synthesizing one last paper to conclude our “Journal Pub” session – I apologise it took so long! I read Karoline Fritzsche and Göran Arnqvist‘s paper “Homage to Bateman: sex roles predict sex differences in sexual selection”, published in Evolution in 2013.

In this paper the authors review the classic sex-role theory, which assumes sexual selection to be stronger in males in taxa with conventional sex roles (systems where the females are the choosy sex and contests for mates are mainly between males) and in females in systems with reversed sex roles. Little empirical work has been done to assess the relative strength of sexual selection on males and females, and no previous study has been able to provide measures in order to compare the strength of this process between sexes and between different taxa. For example, research is often limited to comparing sexual dimorphic traits between the two sexes of a species to evaluate the asymmetry of selection between males and females. The challenges of this type of study are reinforced by the debate regarding what type of measure should be used to quantify the strength of sexual selection (Fitze and Le Galliard 2011). To address these knowledge and evidence gaps, Fritzsche and Arnqvist aim to (i) clarify whether there is a single measure that is best for quantifying sexual selection, (ii) determine if it is best to base measures of sexual selection on phenotypic traits or variance across individuals, and finally (iii) assess how important is it to quantify the strength of sexual selection in both males and females.

The authors discuss these issues by presenting an experiment in which they observed the mating behaviour and reproductive success of both sexes of four seed beetle species. They used four related species of beetles: two of the Callosobruchus genus, females of which are the choosy sex, and two of the Megabruchidius genus, where females often compete against each other for mates.  Fritzsche and Arnqvist then attempted to compare the relative strength of sexual selection between the two sexes, and test the validity of various measures such as variance-based measures – measures unrelated to differences between morphological traits, like Bateman gradients (which they also refer to as sexual selection gradients: these are estimates of the slope of a regression line of reproductive success on mating success, and therefore describe how much fitness each individual gains per successful mating) and the opportunity for sexual selection (variance in reproductive success). Other measures analysed by the authors were trait-based measures like the selection differential (covariance between a standardized trait and fitness), the mating differential (covariance between a standardized trait and mating success), and the residual selection differential (covariance between a standardized trait and the residual reproductive success calculated from the Bateman gradient).

The authors used body size as the trait against which to compute selection. They made this choice because body size tends to covary positively with mating success, and also because it is a comprehensive measure that reflects both phenotypic and genetic variation. Furthermore, the conspicuous sexual dimorphism in the seed beetles strongly suggests a history of sexual selection on this trait. In their mating trials, they presented five females to five males, four of which were sterile. Therefore, each mating assay yielded data on mating and reproductive success for all the females and only one male. The authors quantified mating success by observing how many times each individual was successful at mating, female reproductive success by counting how many offspring each of them produced, and male reproductive success by summing all the offspring produced by the five females in his assay group (which are necessarily the offspring of the lone fertile male).

The Bateman gradients were identified as the best measure to quantify the strength of sexual selection for comparisons between sexes and/or across species. This study’s results support the idea that variance-based measures of sexual selection are very accurate at representing the sexual dimorphism (behavioural and morphological) of these species of beetles. Indeed, Bateman gradients show both male and female mating adaptations, since changes in adaptations are depicted by changes in gradients, representing the properties of the specific mating system. Bateman gradients were identified as the most relevant because they were very good predictors of sexual dimorphism of both secondary sexual traits and mating behaviour across the different species. Bateman gradients were generally steeper in males than in females, and steeper in species with species where males are the choosy sex (Figure 1A). In Callosobruchus species sexual dimorphism was more pronounced, as were the male and female Bateman gradients. In contrast, the opportunity for sexual selection was larger in males of Callosobruchus species, in which females are choosy, but similar or stronger in females of species where the males are choosy (Figure 1B).




Figure 1. The different Bateman values and opportunity for sexual selection for the different species of seed beetles. CM = C. maculatus; CC = C. chinesis; MD = M. dorsalis; MT = M. tonkineus; white bars represent males, black bars represent females. SRR+ indicates sex-role-reversed species and SRR− denotes species with conventional sex roles. Error bars = SE (Figure by Fritsche and Arnqvist 2013).

The authors’ results are consistent with the classic sex role theory, as the calculated Bateman gradients support that the strength of sexual selection is greater in males than in females. The strength of sexual selection varied with mating system. Sex role reversal is often associated with male provision of nutritious gifts to females, increasing female direct benefits with mating success and thereby increasing the female Bateman gradient in such systems. Indeed, male Megabruchidius provide nutritious ejaculates to females, which directly increase the number of eggs a female lays (Takakura 1999). In contrast, there is no conspicuous benefit to additional matings beyond the first one among female Callosobruchus (Arnqvist et al. 2005).

The authors argue that, in the absence of a trade-off between male nuptial gift provisioning and mating success, increased male nuptial gift-giving should increase the Bateman gradients not only of females but also of males. As expected, in this study the Bateman gradients of gift-giving males (Megabruchidius spp.) were the highest. Moreover, even though one might predict that in the Megabruchidius species, female Bateman gradients would be steeper than those of males (because of the sex-role-reversal), this does not necessarily need to be the case. Indeed, stronger sexual selection on females requires a male trade-off between mating success and pre-copulatory fertilization success, which is likely to occur under low resource levels due to the costliness of mating and of providing a nuptial gift. However, this trade-off could have been affected by the experimental design, because the provision of ad libitum food may have provided the male beetles with greater energy levels that they would have in nature. Also, the study males varied in resource acquisition, a fact that could have further weakened the potential trade-off, or perhaps made it harder to detect experimentally. Despite these issues, the higher sexual selection opportunity in female Megabruchidius (Figure 1B) conforms to the sex-role-reversed system.

The authors discuss the importance of post-copulatory sexual selection, which is mediated by female cryptic choice and/or sperm competition. This type of selection is an important component of the sexual selection acting on seed beetles. Residual selection is a measure of the “strength of selection on a trait due to factors other than mating success”, and is calculated as the covariance between a standardized trait and the residual reproductive success obtained from the Bateman gradient. Residual selection has been regarded as a measure of post-copulatory sexual selection and/or fecundity selection based on a trait (z)under sexual selection (in the case of this study, body size), including components from both natural (e.g. fecundity) and sexual selection (e.g. sperm competition). In males, this measure represents the covariance of z with both fecundity and success in sperm competition. Instead, female residual selection represents only the covariance of z and female fecundity.

Fritzsche and Arnqvist conclude their paper by highlighting how the data they gathered, and the measures of strength of sexual selection they calculated, were consistent with the sexual dimorphisms in behaviour and morphology in the studied species of seed beetles. Variance-based measures appeared to be more accurate at representing the sexual dimorphisms observed across the different beetle species. Bateman gradients in particular were the most informative measure of the strength of sexual selection, allowing comparisons between sexes and across species. However, the authors underline the importance of gathering data from both pre- and post-copulatory reproductive competition to provide deeper knowledge on how variation in the strength of sexual selection within and across species affects mating systems.



Reviewed paper: Fritzsche, K., Arnqvist, G., 2013. Homage to Bateman: sex roles predict sex differences in sexual selection. Evolution67(7): 1926–1936.

Arnqvist, G., Nilsson, T., Katvala, M., 2005. Mating rate and fitness in female bean weevils. Behavioural Ecology16: 123–127.

Fitze, P. S., Le Galliard, J. F., 2011. Inconsistency between different measures of sexual selection. American Naturalist178: 256–268.

Takakura, K., 1999. Active female courtship behavior and male nutritional contribution to female fecundity in Bruchidius dorsalis (Fahraeus) (Coleoptera : Bruchidae). Researches on Population Ecology41: 269–273.



Kokko, Klug & Jennions, 2012: Unifying cornerstones of sexual selection: operational sex ratio, Bateman gradient and the scope for competitive investment

This paper uses formal theory to further explore the circumstances (in terms of sex ratios or sex differences in time spent in or out of the mating pool) that favour investment in costly competitive traits.  The authors consider why neither of two commonly used concepts for explaining variation in sexual selection (and previously discussed in Journal Pub), the operational sex ratio (OSR) and the Bateman gradient, are consistently good predictors of mating system.  Kokko and colleagues suggest that both measures provide complementary information about a mating system, and that a more complete approach to explain variation in sexual selection would be to consider both measures, because the Bateman gradient describes the fitness gain per mating and the OSR measures the potential difficulty in obtaining mates.

Kokko et al.’s model adds investment costs to survival into existing mating system theory (“time-in, time out” of the mating pool framework; Clutton-Brock & Parker, 1992; Kokko & Jennions, 2008; Kokko & Monaghan, 2001; Kokko & Ots, 2006), to examine why the strength of sexual selection does not always covary with OSR, despite greater variance in male mating success as the OSR becomes more male-biased.  They integrate measures of the OSR and Bateman’s principles with investment theory, then predict whether a costly trait that increases mating rate will evolve.  Kokko et al. describe the relative importance of investment in mating rate as the scope for competitive investment (SCI): this metric conveniently assesses how much investment an individual ought to make in elevating mating success relative to other fitness components.

The paper draws three general conclusions:

Conclusion 1. If individuals of a given sex have a very short dry time, then the scope for competitive investment becomes large – irrespective of the OSR.”(Kokko, Klug, & Jennions, 2012)

When time away from mating pool is brief (short dry time) for males, the scope for competitive investment is large and it will eventually cause the OSR to become male biased.  However the OSR is not always male-biased when the SCI for males is high. When male dry time remains short, it’s still worth investing in competitive traits in situations where there are many females (males are not mate limited) as males get large benefits regardless (figure 1).  If the only route to increase fitness for males is by increasing their mating rate (alternative routes such as investing in parental care are not available, so dry time remains short), then males will invest in increasing their mating rate regardless of the competitive environment in which they find themselves.  For females (with dry times ranging from short to long) it is only worth investing in competitive traits (high SCI) when the OSR is female-biased (figure 1).

Figure 1 The scope for competitive investment and Bateman differential (insert) for males (solid line) and females (dashed line) when male dry time is short and female dry time varies.  OSR varies from female biased to male biased.  Figure from Kokko et al. 2012.

Figure 1 The scope for competitive investment and Bateman differential (insert) for males (solid line) and females (dashed line) when male dry time is short and female dry time varies. OSR varies from female biased to male biased. Figure from Kokko et al. 2012.

Conclusion 2. When the dry time of one sex varies from short to long, we expect a positive relationship between the OSR and the SCI in this sex.”(Kokko et al., 2012)

When time away from the mating pool (dry time) is not restricted in males, and instead varies from short to long, for example if males invest increasingly more time to parental care, the scope for investing in the evolution of competitive traits is reduced as dry time increases, and intensified by mate limitation (male-biased OSR) (see figure 2).

Figure 2 The scope for competitive investment and Bateman differential (insert) for males (solid line) and females (dashed line) when male dry time varies from short to long and female dry time is long.  OSR varies from female biased to male biased.  Figure from Kokko et al. 2012.

Figure 2 The scope for competitive investment and Bateman differential (insert) for males (solid line) and females (dashed line) when male dry time varies from short to long and female dry time is long. OSR varies from female biased to male biased. Figure from Kokko et al. 2012.

At female-biased OSRs there is high scope for the evolution of female competitive traits, because an indirect effect of increasing male dry time is to decrease female mating rate (as males are removed from the pool).  In this scenario OSR is a good predictor of mating system.

Conclusion 3. If other life-history aspects vary, it is difficult to make simple predictions about investment in competitive traits based solely on the OSR.”(Kokko et al., 2012)

Kokko and colleagues illustrate how when comparing study systems that differ in one or more life history trait or population parameter, OSR is not always good predictor of mating system (figure 3).  They consider the scope for evolution of male competitive traits under three mate encounter rate scenarios when sex ratio at maturation varies among species.

Figure 3 The scope for competitive investment and Bateman differential (insert) for males under low (left curve), medium (central curve) and high (right curve) mate encounter rates.  For each mate encounter scenario the sex ratio at maturation varies, resulting in a range of OSR values between female biased and male biased.  Figure from Kokko et al. 2012

Figure 3 The scope for competitive investment and Bateman differential (insert) for males under low (left curve), medium (central curve) and high (right curve) mate encounter rates. For each mate encounter scenario the sex ratio at maturation varies, resulting in a range of OSR values between female biased and male biased. Figure from Kokko et al. 2012

As the OSR becomes more male-biased the benefit of mating increases along with the scope for competitive investment for males (figure 3).  When the SCI, Bateman differential and OSR covary positively it explains why in systems where ‘all else is equal’ OSR can be used as good predictor of investment in competitive traits (if we consider each curve in figure 3 independently).  However, the predictive power of OSR disappears if the species or populations being compared follow different curves, as illustrated by the three mate encounter rate scenarios shown in figure 3. The authors illustrate this problem by comparing two species, A and B that differ in a single population parameter, density (shifting the mate encounter rate); species A has a low mate encounter rate, and species B has a high mate encounter rate.  Even though the SCI, Bateman differential and OSR covary positively for each species, when we compare the scope for the evolution of competitive traits across species we find that species A can have a higher SCI at a female-biased OSR than species B at a male-biased OSR.

The fact that the OSR is only sometimes a good predictor of mating system can perhaps best be explained using a thought experiment.  Kokko et al. ask whether it is worth investing in a sexual trait to increase mating rate despite an arbitrary cost (which they fix in their thought experiment at 30% of longevity).  Figure 4 illustrates three scenarios where individuals differ in the time spent in the mating pool relative to ‘dry time’.

Figure 4 The relationship between the length of dry time and the evolution of a hypothetical trait that triples the mating rate at a cost to 30% of lifespan.  The two series of bars represent time (lifespans of 2 individuals that either do or do not invest in the costly trait); light bars represent time in the mating pool and dark bars represent dry time.  Reproductive success is estimated as the total number of dark bars (completed breeding events).   When dry time is very short (A and B), short-lived individuals achieve greater reproductive success, regardless of OSR (in A the sex-ratio is less skewed towards the focal animal’s sex, because the required time in the mating pool is shorter than in B).  When dry time is long (c), investing in trait to reduce and already short waiting time in the pool does not compensate for the associated cost to lifespan.  Figure from Kokko et al. 2012

Figure 4 The relationship between the length of dry time and the evolution of a hypothetical trait that triples the mating rate at a cost to 30% of lifespan. The two series of bars represent time (lifespans of 2 individuals that either do or do not invest in the costly trait); light bars represent time in the mating pool and dark bars represent dry time. Reproductive success is estimated as the total number of dark bars (completed breeding events). When dry time is very short (A and B), short-lived individuals achieve greater reproductive success, regardless of OSR (in A the sex-ratio is less skewed towards the focal animal’s sex, because the required time in the mating pool is shorter than in B). When dry time is long (c), investing in trait to reduce and already short waiting time in the pool does not compensate for the associated cost to lifespan. Figure from Kokko et al. 2012


In the first scenario (case A) on average the individual spends quite a long while competing in the mating pool and a relatively short time out of the pool after each mating (dry time, presumably when an individual is preoccupied with other activities like refraction, feeding, laying eggs or parental care, and is therefore unable to mate).  In this scenario it is worth investing in a trait that increases mating rate despite an associated cost of a 30% reduction in lifespan, as can be seen by the increase of 4 mating events in the lower pathway of the short lived individual. The second scenario (case B) has an individual spending even longer soliciting mates in the mating pool (representative of an OSR that is even further skewed towards the focal animal’s sex) and a similar dry time to scenario A.  In this scenario it is also worth investing in a costly trait that increases mating rate: the trait increases lifetime reproductive success by two extra mating events.  Case C shows a situation in which the time spent finding a mate is short relative to the time spent outside the mating pool after each mating.  Here the meagre reductions in an already short time in the mating pool that would be conferred by diverting investment from longevity to mating rate are not worth the cost, and investment in sexual traits is therefore not favoured regardless of the OSR.  This work clarifies some otherwise puzzlingly inconsistent empirical patterns in the literature, and provides clear directions for new empirical work, including my own PhD research on mating systems in dance flies.


Clutton-Brock, T., & Parker, G. (1992). Potential reproductive rates and the operation of sexual selection. Quarterly Review of Biology, 67(4), 437–456.

Kokko, H., Klug, H., & Jennions, M. D. (2012). Unifying cornerstones of sexual selection: operational sex ratio, Bateman gradient and the scope for competitive investment. Ecology Letters, 15(11), 1340–51.

Kokko, & Jennions. (2008). Parental investment, sexual selection and sex ratios. Journal of Evolutionary Biology, 21(4), 919–48.

Kokko, & Monaghan. (2001). Predicting the direction of sexual selection. Ecology Letters, 4(2), 159–165. Kokko, & Ots. (2006). When not to avoid inbreeding. Evolution; International Journal of Organic Evolution, 60(3), 467–75.

The Evolution of Parental Care in the Context of Sexual Selection: A Critical Reassessment of Parental Investment Theory (2002) Wade MJ and Shuster SM

Previously discussed papers: Bateman 1948,Trivers 1972, Emlen & Oring 1977 and Arnold & Duvall (1994)

As we arrive at the fifth paper on the topic of mating systems, most of the themes highlighted in the discussion of Trivers’ 1972 paper have made an appearance: timing of investment, risks and rewards of mating strategies, and the influence of female choice. Again, these themes are common throughout Wade and Shuster’s paper, which emphasizes early gamete investment and its latent effects on the behaviour of males and females. Gametes are the first form of investment in offspring, and it is almost always females that invest in gametes the most heavily. Because males invest comparatively little in gametes, they can benefit from mating with multiple females, whereas females have little to gain from multiple sexual encounters, other than possibly an increased chance of successful fertilisation.

Wade and Shuster examine a classic paper by Maynard Smith (1977), which describes an Evolutionarily Stable Strategy (ESS) model. Through this model, Maynard Smith tried to formalize the ideas first articulated by Bateman (linked above); his model involves a nondescript species with typical sex roles, and assumes that re-mating within this species has both costs and benefits.

Maynard Smith’s ESS model shows that under some conditions it is possible to find both males that care for their offspring and females that desert theirs, despite the prevalence of indiscriminate mating in males and choosy behaviour in females. Past ESS models have shown that polymorphic traits, including polymorphisms in mating behaviour, can only evolve in a system if they offer equal fitness to one another. In the context of Maynard Smith’s model, this means that if atypically raised offspring (e.g. deserted by the female, cared for by the male) and those raised only by females (with deserting males) are exactly as viable as one another, the alternative mating behaviours will both be evolutionarily stable and remain.
Wade and Shuster take the ESS model by Maynard Smith and attempt to modify it in light of the state of evolutionary theory in the early 2000s.

In their paper, they argue that Maynard Smith’s model made some critical invalid assumptions. For example, the original model did not take into account how male re-mating could affect female fitness (such as through withdrawal of care for the purpose of remating). To illustrate the problem with such an assumption, they demonstrate that under Maynard-Smith’s model, when the sex ratio was equal, deserting males would be unable to breed with multiple females – either that or deserting males could not exist when the sex ratio was 1:1.

Wade and Shuster added several components to the model to overcome these problems. They add a ‘payoff matrix’ into the model, in which deserters may have more offspring, but these offspring are less likely to reach adulthood, and sacrificing future reproduction to care for current offspring is an opportunity cost. Their model also takes into account the reduced number of available females when deserting males mate multiple times. It therefore considers females a limited resource, meaning deserting males shift the operational sex ratio. Wade and Shuster were able to simplify the model to a single equation.
The deserting strategy would become more common than the caring strategy when:
/2 < p
s is offspring survivorship, and p is the probability of male mating.)

Because each offspring only has half of a parent’s DNA, strategic allocation to care (which increases offspring survivorship, s) must be scaled by half when assessing its value relative to male re-mating opportunities (p). When s/2 < p, desertion should be more prevalent (because fitness returns from re-mating outweigh those of caring), while care should be more prevalent when s/2 > p.

Wade and Shuster note that this solution satisfies the requirement of population genetic theory that male and female fitness should be equal, an important improvement over Maynard-Smith’s original ESS model.

In closing, they note that the presence of polygamous males and caring females under some conditions shows that sex roles can be the cause of differences in parental investment, rather than a consequence of initial differences in investment that are reflected in anisogamy, and that this inversion of the classic understanding “stands parental investment theory on its head”. While this may be a fair synthesis with respect to the conventional shorthand view, it is worth noting Trivers’ acknowledgement of the complex, reinforcing relationship between parental investment and sexual selection. Is this complex, bidirectional, causal relationship ultimately responsible for uncertainty about the causes of diversity in sexual differences among taxa? Maybe subsequent posts can help clarify this…

Arnold & Duvall (1994) Animal Mating Systems: A Synthesis Based on Selection Theory

Arnold & Duvall (1994) use mathematical modeling and statistical analysis of classic data such as those collected by Bateman (1984) to analyse how the strength of sexual selection can be used to explain diversity in mating systems.

The previous papers (by Bateman 1948, Trivers 1972, and Emlen & Oring 1977), discussed in previous posts, had set the stage for more empirical and theoretical work attempting to explain the evolution of mating systems. Arnold & Duvall (1994) suggested that although there had been many important articles contributing to different aspects of mating system theory, including Bateman’s classic work on the relationship between fecundity and mating success, there was no formal theoretical and analytical framework that integrated all the research.

The authors reaffirm that the relationship between mating success and fecundity (based on Bateman’s original work) is a key driver of mating system evolution.  One of the paper’s main themes is based on a now well-accepted idea articulated in the early 1980’s (Lande and Arnold 1983), that selection can be seen as the statistical relationship between certain traits and fitness. To integrate this analytic approach with the study of mating systems, Arnold and Duvall propose a 4 tiered hierarchical framework including the traits that influence fitness. This conceptual model illustrates the direct and indirect relationships between traits and fitness measures, and allows formal testing of the pathways that affect fitness components. Traits that have the most direct effect on fitness are assigned rank one, while more indirect agents have higher ranks (2, 3 or 4) depending on the number of presumed mediating factors that relate them with fitness (Figure 1.).

Luc noted that creating thought maps or path diagrams similar to this figure, which describe the important relationships or factors within a system, could be very useful in allowing us to visualize and understand the important questions in our own research. These conceptual diagrams often further allow one to make the statistical associations between correlated components of a system more explicit.

Arnold and Duvall explain how the ‘selection gradients’ illustrated as arrows in Figure 1 can be quantified using multiple regression of fitness on estimates of the traits presumed to be under selection. Each aforementioned selection gradient is the partial standardized regression coefficient in a multiple regression including other aspects of the phenotype. Multiple regression can therefore be used to estimate the total combined selection on all the various traits affecting fitness, including the sexual selection component that affects reproductive fitness.

The authors explain that linear regression is appropriate in the estimation of selection gradients even if the fits are nonlinear. This is now an accepted convention when trying to measure strength of selection on a trait, however Luc suggested that, notwithstanding Arnold and Duvall’s logic about the nature of evolutionary genetic change and its relationship with the well-established body of work on selection analysis, we should neverthelessalways question exactly what coefficients mean when they come from a model that might have a poor fit.

The authors further discuss how estimates of selection gradients can be used to test sexual selection theory, by integrating different aspects of mating systems such as nuptial gifts or parental care, to examine the strength of selection on males and females. They argue that their approach quantifies differences in the strength of selection (regression slopes) between males and females, which is useful for testing theory on mating systems.

They illustrate their analysis using several examples of mating systems, including one in which males provide nuptial gifts to females. In this case, models showed that there should be a small increase in female’s selection gradient (strength of sexual selection) for each multiple mating (as a result of the benefits to gaining extra gifts and therefore nutrition), and that the greater the nutritional benefit of the gift, the greater the strength of sexual selection will be.

Arnold and Duvall finally use models involving encounter rate, similar to the ideas proposed by Emlen and Oring (1977), and show that these can also be used to measure the strength of selection on fitness based traits. They do however contest Emlen and Oring’s (1977) assertion about the most useful metric for describing or determining mating systems. Whereas Emlen and Oring argue that the operational sex ratio (the average over time of the number of sexually active males to the number of females capable of insemination) is the most useful indicator of the mating system, Arnold and Duvall reason that the breeding sex ratio (the ratio of breeding males to breeding females, including the zero fecundity class for each sex) is more appropriate. This may be something to think about for some members of our lab who are looking at malaise trap samples to determine the adult operational sex ratios and mating rates of dance flies.

Ultimately the authors claim that it is the disparity in selection gradients that determines which sex competes for access to the other. While sexual selection due to competition will therefore determine a species’ mating system, it seems logical that a species mating system will also influence the level of selection in a cyclical fashion. This reminds us of Trivers (1972), who noted the cyclical relationship between mate competition and parental investment in his own analysis of what determines the sex roles.

Emlen & Oring 1977: Ecology, Sexual Selection, and the Evolution of Mating Systems

The previous posts from our discussions on classic mating systems papers have shown how both empirical work and theory advanced knowledge of sex differences in the returns from relative investment in reproduction. In their 1977 paper, Emlen & Oring attempted to bring natural history observations and ecology into a general theory of mating systems evolution, and to discuss the ecological factors and selective forces that shape polygamous mating systems. Of particular relevance here is Trivers’ work on parental care, as the prevalence of polygamy is often related to whether one sex is freed from parental care duties (and thus have excess time and energy to seek additional mates).

‘Ecology, Sexual Selection, and the Evolution of Mating Systems’ was published 2 years after E. O. Wilson’s ‘Sociobiology’ had hit the shelves, and Emlen & Oring are careful to note early on that understanding mating systems requires the reader to abandon any thoughts of group- or species-level ‘adaptiveness’. Fitness is a measure of the reproductive success of an individual (or genotype) relative to other individuals (or genotypes) in the same or other populations, and so we must consider selection to be operating at the level of the individual . Intraspecific competition is a crucial aspect of sexual selection: essentially, when one sex becomes a limiting factor for the other, the result is an increase in intrasexual competition among members of the available sex for access to mates of the limiting sex. The authors hypothesise that an important cause of the differing intensities of sexual selection found both across species and between populations of the same species is “the ability of a portion of the population to control the access of others to potential mates”. This control may be enforced through physically excluding other members of the same sex from potential mates, or through controlling critical resources. Central to Emlen & Oring’s argument is a cost-benefit analysis: under what environmental circumstances is the defending of multiple mates, or of those resources necessary for gaining multiple mates, economically viable?

Two of the crucial components of this concept of an environment’s ‘polygamy potential’ are illustrated by the figure below, in which the height of the shaded area perpendicular to each diagonal line indicates the environmental potential for polygamy in relation to the spatial distribution of resources (on the x-axis) and the temporal availability of receptive mates (on the y-axis). Resource ‘clumping’ in space means individuals can monopolise critical resources, which always increases the potential for polygamy. Asynchrony of mate availability is required for polygamy, else the time to locate, attract or copulate will mean that other potential mates are no longer available. However, too much asynchrony means the cost of continual defence outweighs the benefits of gaining additional mates.


The environmental potential for polygamy, relative to the spatial distribution of resources and temporal availability of receptive mates. Taken from Emlen & Oring (1977).

Another crucial piece of the sexual selection intensity puzzle is the realisation that the overall ratio of males to females in the population is less important than the operational sex ratio (OSR): the average ratio of fertilisable females to sexually active males at any point. The OSR is affected by spatial and temporal clumping of the limiting sex; the example given is of continuous long periods of male sexual activity alongside brief, asynchronous periods of female receptivity, producing a strong skew in the OSR.

The bulk of the paper outlines an ecological classification of mating systems, concentrating on whether and how access to potential mates and resources are controlled, and the effects of temporal and spatial clumping on the OSR. Detailed examples of mating system types are illustrated using examples of avian mating biology. Emlen & Oring also consider how changes in ecological parameters might disrupt the environmental potential for polygamy, and indicate that their framework should enable predictions of the form of mating system plasticity that occurs.

Trivers 1972: Parental investment and sexual selection

Continuing the series of classic papers on mating systems, Hazel and I lead some discussion on Bob Trivers’ book chapter on how parental investment relates to the sex roles. Bateman (1948) had already suggested that the difference between the sexes in the returns on investment might be related to anisogamy (the difference in gamete size across the sexes), but Trivers examined (using formal theory rather than empirical experiments) the possible effects of investment in all stages of offspring (not just the gametes themselves). He reasoned that since all kids have two parents, the sex that invests more becomes limiting to the other one. The relative investment of the sexes in their young is therefore the key variable controlling sexual selection.

Trivers was careful to point out that although “investment” can be energetic or metabolic, it doesn’t need to be for his theory to work. For example, risky behaviour like hunting or singing (which could lead to predation or parasitism) is also a form of investment and needs to be part of any calculations comparing the sexes.

Trivers also was careful to notes the circular nature of the relationship between investment and mating system, a theme that will undoubtedly resurface as we continue our tour through classic papers on mating systems: parental investment affects sexual selection (e.g., by controlling which sex is in short supply), but sexual selection also affects parental investment (e.g., by determining how much energy is left for care, for example).

The paper also pointed out a few features of the natural history of mating in animals that were likely to be important (observations whose importance we might be able to confirm with the benefit of hindsight). Here are a few haphazardly selected points that will probably feature in future discussions:

  1. The timing of investment (females usually invest substantially in gametes before mating) creates asymmetry between mating partners in the risk of desertion: males may have invested comparatively little in a clutch after mating and so they risk little by deserting, whereas a female may be trapped into caring for the young or losing all of her investment. Conversely, the risk of cuckoldry is asymmetrical in the opposite direction, because males can rarely be completely certain about paternity in the same way that females can trust their relationship to eggs.
  2. The differential risks and returns on parental investment have important implications for sexual differences in mortality. Trivers spent some time arguing that differences in mortality are not simply a consequence of chromosomal differences (i.e., the fact that in most mammals males are heterogametic), but rather imply adaptive differences in investment in longevity. Whether sexual differences in lifespan are generally adaptive is a continuing focus of quite a lot of research, including by our own Tom H.
  3. Female choice is probably related to some important aspects of paternal investment. Research over the past twenty years on the relative importance of direct and indirect benefits owes much to this initial analysis.
  4. In his closing sentence, Trivers reaffirms one of the fundamental insights that has shaped sexual selection research since this paper:

“Throughout, I emphasize that sexual selection favors different male and female reproductive strategies and that even when ostensibly cooperating in a joint task male and female interests are rarely identical.”

This recognition of sexual conflict would have to wait some time to be fully appreciated, in part because the empirical literature had plenty of work to do in testing Trivers’ theory on how parental investment affects sexual selection. In future posts, perhaps we can assess how much of that work remains to be done.

Bateman 1948: Intra-sexual selection in Drosophila

This is the first of a number of posts on “classic papers” in our new series called Journal Pub .

Our first topic is mating systems, and I have the pleasure of summarizing and commenting on Angus Bateman’s study of sexual selection in Drosophila. In 1948, although ¾ of a century had passed since Darwin published Sexual selection and the descent of man, Bateman (1948) remarked that the evidence that sexual selection explained sexual differences remained circumstantial, and that there was considerable debate concerning the importance of mate competition in producing secondary sex characters. For example, Huxley (1938) argued that monogamous birds with striking secondary sexual differences seemed to display mostly after pair formation (and therefore presumably not in the context of contests at all).

What we now know about the many possible episodes for sexual selection (including for example, the potential for postcopulatory sperm competition and female choice) colours our impression of Huxley’s objections, but at the time Bateman’s empirical approach was probably the only sensible response: could he demonstrate that males and females differ in the potential to gain fitness through mating?

He conducted a classic experiment in which he housed an equal number (either 3 or 5 of each sex) of virgin male and female Drosophila melanogaster together for three or four days, and collected the offspring produced within the fly vials during this time. Because each of his flies carried a unique dominant marker, he was able to unambiguously assign all offspring to their parents, and therefore to retroactively work out the reproductive successes of males and females in his experiment. He first noted that males had much higher variation in fitness than females did: there were more males who had no fitness at all, and a few males had dramatically high fitness. (Note that he did a lot of technical work to make sure that his observations of differences in variance across the sexes were real, and not due to errors in experimental execution or measurement.)

Furthermore, he showed that the relationship between mate number and fitness was much stronger in males than it was in females. The figure below (stolen from his paper) has been reproduced many times to illustrate this key result.

Screen Shot 2013-11-29 at 18.48.09

It’s worth noting that the differences between sexes was much stronger in his last pair of experimental blocks (Series 5 and 6, on the right) than in his first four blocks. The reasons for this discrepancy are not clear, but Bateman speculated that his first four blocks suffered from poor vigour; if weak males could not transfer enough sperm to fertilize all of a female’s eggs, several inseminations would be needed.

The key difference between the sexes therefore was that males can gain a lot from remating, but females usually much less so. If this difference in selection on mating was representative of the general situation in animals, that would explain (as Darwin had suggested) why males so often are the showier, more heavily armed sex: they have more to gain from contests over sex than females do.

In discussing this paper on Tuesday, several people mentioned the very recent (and controversial) publication of work that reanalysed (Snyder & Gowaty 2007) or replicated (Gowaty et al., 2012) Bateman’s classic experiments, criticizing many of the conclusions Bateman had drawn. None of us felt sufficiently well prepared to discuss these in any depth, but perhaps they will be interesting for further reading and discussion another day.

Research Group Meeting Nov. 12, 2013

For the second consecutive week, we were forced to relocate from the Wallace Pub on account of renovations. Instead we met at the Meadowpark. After dealing with minor matters related to our own research projects, we discussed the organization of a new initiative for the research group: Journal Pub (aka Beer Review).

As part of an effort to catch up to some of the information age, we’re devoting ourselves to collectively reading some new and classic papers in several corners of evolutionary biology. We’ll organize our efforts using the newest page on our website: Journal Pub. Navigate there to learn about the topics and papers under discussion prior to a particular Journal Pub session, or go there after a session to see the brief written summaries of the papers as well as some annotations of our discussions on each of them. So there’s a bit of wrangling ahead to wrap our heads around a lot of difficult concepts, but it’s exciting to think that we might collectively learn about some very big and important ideas rather productively and quickly.

The first Journal Pub (location TBC) will occur on Nov 26. I have taken the liberty to assign responsibility for chief and adjunct reviewers of each paper, though naturally anyone can read more than the focal assigned papers. Looking forward to the discussions!