Drying to equilibrium with the air is lethal to most species of animals and plants, making drought (i.e., low external water potential) a central problem for terrestrial life and a major cause of agronomic failure and human famine. Surprisingly, a wide taxonomic variety of animals, microbes, and plants do tolerate complete desiccation, defined as water content below 0.1 g H₂O g⁻¹ dry mass. Species in five phyla of animals and four divisions of plants contain desiccation-tolerant adults, juveniles, seeds, or spores. There seem to be few inherent limits on desiccation tolerance, since tolerant organisms can survive extremely intense and prolonged desiccation. There seems to be little phylogenetic limitation of tolerance in plants but may be more in animals. Physical constraints may restrict tolerance of animals without rigid skeletons and to plants shorter than 3 m. Physiological constraints on tolerance in plants may include control by hormones with multiple effects that could link tolerance to slow growth. Tolerance tends to be lower in organisms from wetter habitats, and there may be selection against tolerance when water availability is high. Our current knowledge of limits to tolerance suggests that they pose few obstacles to engineering tolerance in prokaryotes and in isolated cells and tissues, and there has already been much success on this scientific frontier of desiccation tolerance. However, physical and physiological constraints and perhaps other limits may explain the lack of success in extending tolerance to whole, desiccation-sensitive, multicellular animals and plants. Deeper understanding of the limits to desiccation tolerance in living things may be needed to cross this next frontier.

This review will focus on the acquisition of desiccation tolerance in the resurrection plant Craterostigma plantagineum. Molecular aspects of desiccation tolerance in this plant will be compared with the response of non-tolerant plants to dehydration. Unique features of C. plantagineum are described like the CDT-1 (Craterostigma desiccation tolerance gene-1) gene and the carbohydrate metabolism. Abundant proteins which are associated with the desiccation tolerance phenomenon are the late embryogenesis abundant (=LEA) proteins. These proteins are very hydrophilic and occur in several other species which have acquired desiccation tolerance.

Studies in anhydrobiotic plants have defined many genes which are upregulated during desiccation, but comparable studies in invertebrates are at an early stage. To develop a better understanding of invertebrate anhydrobiosis, we have begun to characterise dehydration-inducible genes and their proteins in anhydrobiotic nematodes and bdelloid rotifers; this review emphasises recent findings with a hydrophilic nematode protein. Initial work with the fungivorous nematode Aphelenchus avenae led to the identification of two genes, both of which were markedly induced on slow drying (90–98% relative humidity, 24 hr) and also by osmotic stress, but not by heat or cold or oxidative stresses. The first of these genes encodes a novel protein we have named anhydrin; it is a small, basic polypeptide, with no counterparts in sequence databases, which is predicted to be natively unstructured and highly hydrophilic. The second is a member of the Group 3 LEA protein family; this and other families of LEA proteins are widely described in plants, where they are most commonly associated with the acquisition of desiccation tolerance in maturing seeds. Like anhydrin, the nematode LEA protein, Aav-LEA-1, is highly hydrophilic and a recombinant form has been shown to be unstructured in solution. In vitro functional studies suggest that Aav-LEA-1 is able to stabilise other proteins against desiccation-induced aggregation, which is in keeping with a role of LEA proteins in anhydrobiosis. In vivo, however, Aav-LEA-1 is apparently processed into smaller forms during desiccation. A processing activity was found in protein extracts of dehydrated, but not hydrated, nematodes; these shorter polypeptides are also active anti-aggregants and we hypothesise that processing LEA protein serves to increase the number of active molecules available to the dehydrating animal. Other LEA-like proteins are being identified in nematodes and it seems likely therefore that they will play a major role in the molecular anhydrobiology of invertebrates, as they are thought to do in plants.

The African chironomid Polypedilum vanderplanki exhibits anhydrobiosis, i.e., the larvae can survive complete desiccation. Recovery rate and trehalose content were investigated in larvae desiccated slowly or at a rate more than 3 times faster. Upon slow desiccation (evaporation rate 0.22 ml day⁻¹) larvae synthesized 38 μg trehalose/individual before complete desiccation, and all of them recovered after rehydration, whereas larvae that were dehydrated quickly (evaporation rate 0.75 ml day⁻¹) accumulated only 6.8 μg trehalose/individual and none of them revived after rehydration. In the pools that are their natural habitat P. vanderplanki larvae make tubes by incorporating detritus or soil with their sticky saliva. This tubular structure is a physical barrier not only to protect the larva from natural enemies but also induces successful anhydrobiosis by reducing the dehydration rate. When larvae were dehydrated with 100 μl distilled water (DW) in soil tubes, they accumulated 37 μg trehalose/individual and more than half of them could revive after rehydration, whereas larvae without tubes accumulated lower level of trehalose and none recovered after rehydration.

Encysted embryos (cysts) of the primitive crustacean, Artemia franciscana, are among the most resistant of all animal life history stages to extremes of environmental stress. These embryos, extremophiles of the animal kingdom, are the main focus of this paper. Previous work has revealed the importance of biochemical and biophysical adaptations that provide a significant part of the basis of their resistance, and I consider some of these here. In the present paper the critical role played by the outer layer of the shell in desiccation tolerance will be one focus. Another involves studies on the response of dried cysts to high temperatures that, among other things, implicate one or more volatile factors released from the cysts that determines the extent of thermotolerance under a given heating regime. A hypothetical scheme is given to account for these peculiar results. Based on western immunoblotting analysis, and data from the literature, the scheme also implicates the heat-induced translocation of the stress protein p26 to nuclei as a potential cause of the reduction in hatching level.

Desiccation tolerance is a wide-spread phenomenon in the plant kingdom, particularly in small propagules lacking own root or rhizome system, such as seeds, pollen, spores of spore plants, and whole moss plants, but rare in whole, vascular plants. Longevities in the desiccated state vary from a few days in some pollen and spore types to many decades in some seeds and moss spores, green vegetative tissues being intermediate in that respect. Therefore, small size of a propagule does not appear to be a factor limiting life span. The formation of a glassy state in the cytoplasm upon water loss considerably increases viscosity and slows deteriorative chemical reactions. Intermolecular hydrogen bonding strength and length in the glassy cytoplasm have been suggested to play a role in desiccation tolerance and longevity. To further explore this, a comparative Fourier transform IR study among dried anhydrobiotic plant propagules belonging to different phyla was conducted. This study indicated that strong hydrogen bonding does not correlate with long life span, but rather depends on the composition of the glass forming compounds. By contrast, a large number of double bonds in the acyl chains of the polar lipids correlated with short life span. This result suggests that deteriorative processes in membranes rather than in the glassy cytoplasm determine the rate of aging of dried anhydrobiotic propagules. This would agree with the view that lipids form the only fluid or semi-fluid phase in the dried propagules, which renders them comparatively susceptible to free radical attack.

Most organisms depend on the availability of water. However, some life-forms, among them plants and fungi, but very few animals, can survive in the desiccated state. Here we discuss biochemical mechanisms that confer tolerance to desiccation in photosynthetic and non-photosynthetic organisms. We first consider damage caused by water removal and point out that free radicals are a major cause of death in intolerant tissue. Free radicals impair metabolism and necessitate protection and repair during desiccation and rehydration, respectively. As a consequence, desiccation tolerance and prolonged longevity in the desiccated state depend on the ability to scavenge free radicals, using antioxidants such as glutathione, ascorbate, tocopherols and free radical-processing enzymes. Some ‘classic’ antioxidants may be absent in lower plants and fungi. On the other hand, lichens and seeds often contain secondary phenolic products with antioxidant properties. The major intracellular antioxidant consistently found in all life forms is glutathione, making it essential to survive desiccation. We finally discuss the role of glutathione to act as a signal that initiates programmed cell death. The failure of the antioxidant system during long-term desiccation appears to trigger programmed cell death, causing ageing and eventual death of the organism. In turn, this suggests that a potent antioxidant machinery is one of the underlying mechanisms of desiccation tolerance.

Soil nematodes are capable of employing an anhydrobiotic survival strategy in response to adverse environmental conditions. The McMurdo Dry Valleys of Antarctica represent a unique environment for the study of anhydrobiosis because extremes of cold, salinity, and aridity combine to limit biological water availability. We studied nematode anhydrobiosis in Taylor Valley, Antarctica, using natural variation in soil properties. The coiled morphology of nematodes extracted from dry valley soils suggests that they employ anhydrobiosis, and these coiled nematodes showed enhanced revival when re-hydrated in water as compared to vermiform nematodes. Nematode coiling was correlated with soil moisture content, salinity, and water potential. In the driest soils studied (gravimetric water content <2%), 20–80% of nematodes were coiled. Soil water potential measurements also showed a high degree of variability. These measurements reflect microsite variation in soil properties that occurs at the scale of the nematode. We studied nematode anhydrobiosis during the austral summer, and found that the proportion of nematodes coiled can vary diurnally, with more nematodes vermiform and presumably active at the warmest time of day. However, dry valley nematodes uncoiled rapidly in response to soil wetting from snowmelt, and most nematode activity in the Dry Valleys may be confined to periods following rare snowfall and melting events. Anhydrobiosis represents an important temporal component of a dry valley nematode's life span. The ability to utilize anhydrobiosis plays a significant role in the widespread distribution and success of these organisms in the Antarctic Dry Valleys and beyond.

Persistence of anhydrous organisms in nature may depend on how long they remain viable in dry environments. Longevity is determined by interactions of humidity, temperature, and unknown cellular factors that affect the propensity for damaging reactions. Here we describe our research to elucidate those cellular factors and to ultimately predict how long a population can survive under extreme conditions. Loss of viability typically follows a sigmoidal pattern, where a period of small changes precedes a cataclysmic decline. The time for viability to decrease to 50% (P50) varied among seed species and among 10 phylogenetically diverse organisms. When stored at elevated temperatures of 35°C and 32% relative humidity (RH), P50 ranged from about a week for spores of Serratia marcescens to several years for fronds of Selaginella lepidophylla. Most of the species studied survived longest at low humidity (10–20% RH), but suffered under complete dryness. Temperature dependencies of aging kinetics appeared similar among diverse organisms despite the disparate longevities. The effect of temperature on seed aging rates was consistent with the temperature dependency of molecular mobility of aqueous glasses, with both showing a reduction by several orders of magnitude when seeds were cooled from 60°C to 0°C. Longevity is an inherited trait in seeds, but its complex expression among widely divergent taxa suggests that it developed through multiple pathways.

Bdelloid rotifers are aquatic microinvertebrates common in water bodies and in unstable “terrestrial” habitats, such as mosses and lichens. The key to the adaptability to live in unstable habitats is their capacity to tolerate habitat desiccation through anhydrobiosis, that is assumed apomorphic to the taxon. The life history traits of some “moss” and “water” species of bdelloid are compared, showing that the water species have shorter life span, higher fecundity and earlier age at first reproduction than the moss species. These traits are discussed in the light of current life history theories. Contrary to the assumptions of the models, anhydrobiosis of bdelloids does not appear to imply energy demand. Past research on bdelloid anhydrobiosis is briefly reviewed, focusing on the factors that affect anhydrobiosis success, like morphological and physiological adjustments, and on the effect of events of anhydrobiosis during life time. Desiccation produces a time shift on the age of the bdelloid, which disregards the time spent as anhydrobiotic, following the so-called “Sleeping Beauty” model. Average fecundity is never found to decrease as a consequence of anhydrobiosis, but is either equal or even higher than that of a hydrated rotifer. Bdelloid populations seem to benefit from anhydrobiosis; fitness of a bdelloid is found to decline, if populations are maintained hydrated for several generations, but not if populations are cyclically desiccated. We hypothesize that anhydrobiosis can be an essential event for long-term survival of bdelloid populations.

The life histories of holo-anhydrobiotic animals differ from those of all other organisms by a regular or irregular entrance into an ametabolic state induced by desiccation. Such ametabolic periods will arrest growth and reproduction completely and thus affect primary life history parameters dramatically. The selective forces and the genetic and physiological trade-offs acting on anhydrobiotic animals are to a large extent unknown. Assuming low growth rates and low juvenile to adult survival, general theoretical models on life history responses to stress predict that anhydrobiotic animals will be selected for a high degree of iteroparity, with low fecundity, large egg size, and low total reproductive investment. A high degree of variability in growth and reproduction should create a selective force in the same direction. Although basic empirical data on life history parameters are very scarce, available observations seem to be consistent with this prediction.

Desiccation-tolerance in vegetative tissues of angiosperms has a polyphyletic origin and could be due to 1) appropriation of the seed-specific program of gene expression that protects orthodox seeds against desiccation, and/or 2) a sustainable version of the abiotic stress response. We tested these hypotheses by comparing molecular and physiological data from the development of orthodox seeds, the response of desiccation-sensitive plants to abiotic stress, and the response of desiccation-tolerant plants to extreme water loss. Analysis of publicly-available gene expression data of 35 LEA proteins and 68 anti-oxidant enzymes in the desiccation-sensitive Arabidopsis thaliana identified 13 LEAs and 4 anti-oxidants exclusively expressed in seeds. Two (a LEA6 and 1-cys-peroxiredoxin) are not expressed in vegetative tissues in A. thaliana, but have orthologues that are specifically activated in desiccating leaves of Xerophyta humilis. A comparison of antioxidant enzyme activity in two desiccation-sensitive species of Eragrostis with the desiccation-tolerant E. nindensis showed equivalent responses upon initial dehydration, but activity was retained at low water content in E. nindensis only. We propose that these antioxidants are housekeeping enzymes and that they are protected from damage in the desiccation-tolerant species. Sucrose is considered an important protectant against desiccation in orthodox seeds, and we show that sucrose accumulates in drying leaves of E. nindensis, but not in the desiccation-sensitive Eragrostis species. The activation of “seed-specific” desiccation protection mechanisms (sucrose accumulation and expression of LEA6 and 1-cys-peroxiredoxin genes) in the vegetative tissues of desiccation-tolerant plants points towards acquisition of desiccation tolerance from seeds.

Bryophytes are a non-monophyletic group of three major lineages (liverworts, hornworts, and mosses) that descend from the earliest branching events in the phylogeny of land plants. We postulate that desiccation tolerance is a primitive trait, thus mechanisms by which the first land plants achieved tolerance may be reflected in how extant desiccation-tolerant bryophytes survive drying. Evidence is consistent with extant bryophytes employing a tolerance strategy of constitutive cellular protection coupled with induction of a recovery/repair mechanism upon rehydration. Cellular structures appear intact in the desiccated state but are disrupted by rapid uptake of water upon rehydration, but cellular integrity is rapidly regained. The photosynthetic machinery appears to be protected such that photosynthetic activity recovers quickly. Gene expression responds following rehydration and not during drying. Gene expression is translationally controlled and results in the synthesis of a number of proteins, collectively called rehydrins. Some prominent rehydrins are similar to Late Embryogenesis Abundant (LEA) proteins, classically ascribed a protection function during desiccation. The role of LEA proteins in a rehydrating system is unknown but data indicates a function in stabilization and reconstitution of membranes. Phylogenetic studies using a Tortula ruralis LEA-like rehydrin led to a re-examination of the evolution of desiccation tolerance. A new phylogenetic analysis suggests that: (i) the basic mechanisms of tolerance seen in modern day bryophytes have changed little from the earliest manifestations of desiccation tolerance in land plants, and (ii) vegetative desiccation tolerance in the early land plants may have evolved from a mechanism present first in spores.

The loss of water from cells is a stress that was likely imposed very early in evolution. An understanding of the sensitivity or tolerance of cells to depletion of intracellular water is relevant to the study of quiescence, longevity and aging, because one consequence of air-drying is full metabolic arrest, sometimes for extended periods. When considering the adaptation of cells to physiological extremes of pH, temperature or pressure, it is generally assumed that evolution is driven toward optimum function rather than maximum stability. However, adaptation to desiccation has the singular and crucial distinction that dried cells do not grow, and the time the cell is dried may represent the greater part of the life (the time the cell remains viable) of that cell and its component macromolecules. Is a consideration of “function” relevant in the context of desiccated cells? The response of prokaryotic cells to desiccation, and the mechanisms they employ to tolerate this stress at the level of the cell, genome and proteome are considered. Fundamental principles were then implemented in the design of strategies to achieve air-dry stabilization of sensitive eukaryotic (human) cells. The responses of the transcriptomes and proteomes of prokaryotic cells and eukaryotic cells (yeast and human) to drying in air are compared and contrasted to achieve an evolutionary context. The concept of the “desiccome” is developed to question whether there is common set of structural, physiological and molecular mechanisms that constitute desiccation tolerance.

The Center for Biostabilization at UC Davis is attempting to stabilize mammalian cells in the dry state. We review here some of the lessons from nature that we have been applying to this enterprise, including the use of trehalose, a disaccharide found at high concentrations in many anhydrobiotic organisms, to stabilize biological structures, both in vitro and in vivo. Trehalose has useful properties for this purpose and in at least in one case—human blood platelets—introducing this sugar may be sufficient to achieve useful stabilization. Nucleated cells, however, are stabilized by trehalose only during the initial stages of dehydration. Introduction of a stress protein obtained from an anhydrobiotic organism, Artemia, improves the stability markedly, both during the dehydration event and following rehydration. Thus, it appears that the stabilization will require multiple adaptations, many of which we propose to apply from studies on anhydrobiosis.

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.

I introduce the term “Darwin-Bateman Paradigm” to include several proposals stemming from the writings of Charles Darwin and A. J. Bateman, including the notions that (a) male reproductive success is more variable than that of females, (b) males gain more in reproductive success from repeated matings than do females, and (c) males are generally eager to mate and relatively indiscriminate whereas females are more discriminating and less eager. I trace this paradigm from Darwin's The Descent of Man through Bateman's research and beyond. I try to clarify the terminology used in applying Bateman's results and discuss both the impact and the criticisms the paradigm has engendered. I then broaden the context of the Darwin-Bateman Paradigm to show related conceptions in disparate fields that evolved in parallel with it. I conclude that gender stereotypes appear to have influenced these conceptions. The paradigm has been of great heuristic value but is in need of further empirical investigation in view of numerous exceptions to these general rules.

Bateman's principle predicts the intensity of sexual selection depends on rates of increase of fecundity with mating success for each sex (Bateman slopes). The sex with the steeper increase (usually males) is under more intense sexual selection and is expected to compete for access to the sex under less intense sexual selection (usually females). Under Bateman and modern refinements of his ideas, differences in parental investment are key to defining Bateman slopes and thus sex roles. Other theories predict sex differences in mating investment, or any expenditures that reduce male potential reproductive rate, can also control sex roles. We focus on sexual behaviour in systems where males have low paternal investment but frequently mate only once in their lifetimes, after which they are often killed by the female. Mating effort (=terminal investment) is high for these males, and many forms of investment theory might predict sex role reversal. We find no qualitative evidence for sex role reversal in a sample of spiders that show this extreme male investment pattern. We also present new data for terminally-investing redback spiders (Latrodectus hasselti). Bateman slopes are relatively steep for male redbacks, and, as predicted by Bateman, there is little evidence for role reversal. Instead, males are competitive and show limited choosiness despite wide variation in female reproductive value. This study supports the proposal that high male mating investment coupled with low parental investment may predispose males to choosiness but will not lead to role reversal. We support the utility of using Bateman slopes to predict sex roles, even in systems with extreme male mating investment.

Many studies have addressed sexual selection in animals, but few data are available on animals that release eggs and sperm into the environment for external fertilization. Although this reproductive mode represents the ancestral condition and is still a very common reproductive strategy, it is underrepresented in empirical studies and theoretical treatments. Here I present data on the pattern of reproductive success in male and female sea urchins. The results suggest that the strength of sexual selection and the differences between the sexes in the intensity of sexual selection depend on mate density. In general, despite the high degree of multiple paternity, the variance in reproductive success appears to be lower in males and higher in females than it is in polygamous species with internal fertilization. These results may provide insight into the patterns of effective population size in marine invertebrates and also more generally the evolutionary transition from sexual monomorphism to polymorphism in adult traits.

Bateman's principle states that reproductive success is limited a) in females by the resources available for egg production; and b) in males, only by access to females and/or eggs. The principle has been used to generate predictions for two aspects of hermaphroditism; a) the advantage of hermaphroditism and b) sexual conflict. Comparing these predictions to the empirical data offers tests of Bateman's principle. Charnov's prediction that hermaphroditism would occur under circumstances where Bateman's principle does not apply is found to be largely correct. However, the prediction as to the association of hermaphroditism and low fixed costs is inconsistent with the data. Alternative explanations that predict that hermaphroditism is a strategy for reducing variance in reproductive success may better explain the data. Probability theory demonstrates that where two strategies have equal mean fitness, which must be the case for male and female function, the strategy with the lower variance in reproductive success must have higher fitness (Gillespie's principle). Bateman's principle predicts that this will be the female role in hermaphrodites. However, Charnov, assuming Bateman's principle, predicted that sexual conflict stemming from a preference for the male role would be important in hermaphrodite mating systems, creating a paradox. Many hermaphrodite mating systems are based on conditional reciprocity with a preferred sexual role indicating sexual conflict. The data demonstrate that the preferred role varies among taxa, contrary to the predictions of Bateman's principle. It has been suggested that Bateman's principle can explain cases in which the female role is preferred (sperm-trading) as involving energy rather than gamete trading. However, energetic considerations suggest that energy trading would only be adaptive if Bateman's principle does not apply, paradoxically. The gamete trading model, based on the prediction that the role that offers control of fertilization will be preferred, is more consistent with the data. Application of Bateman's principle to hermaphrodites leads to contradictory predictions and does not offer the basis for a coherent theory of sexual selection, as Bateman proposed.

Angus J. Bateman's classic study of sexual selection in Drosophila melanogaster has had a major influence on the development of sexual selection theory. In some ways, Bateman's study has served a catalytic role by stimulating debate on sex roles, sexual conflict and other topics in sexual selection. However, there is still considerable disagreement regarding whether or not “Bateman's principles” are helpful in the study of sexual selection. Here, we test the idea that Bateman's principles provide the basis for a useful method to quantify and compare mating systems. In this study, we focus on the sex-role-reversed pipefish Syngnathus typhle as a model system to study the measurement of sexual selection. We set up artificial breeding assemblages of pipefish in the laboratory and used microsatellite markers to resolve parentage. Three different sex-ratio treatments (female-biased, even and male-biased) were used to manipulate the expected intensity of sexual selection. Measures of the mating system based on Bateman's principles were calculated and compared to the expected changes in the intensity of sexual selection. We also compare the results of this study to the results of a similar study of Bateman's principles in the rough-skinned newt, a species with conventional sex roles. The results of this experiment show that measures of the mating system based on Bateman's principles do accurately capture the relative intensities of sexual selection in the different treatments and species. Thus, widespread use of Bateman's principles to quantify mating systems in nature would facilitate comparative studies of sexual selection and mating system evolution.

Bateman demonstrated differences in variance for fertility and mating success between the sexes, with males usually having a greater variance than females. Thus in general, male reproductive success increases with number of mates acquired. These results have been referred to as “Bateman's principles” and taken together with other parameters (e.g., relative parental investment) have been proposed to estimate a component of sexual selection. For this review I examine patterns of parental care and sexual selection in teleost fishes (substrate brooding and with internal fertilization). I present data for the pumpkinseed sunfish Lepomis gibbosus, in which I estimated cost of paternal care and compared direct measures of the intensity of selection on possible sexually selected traits to measures of sexual selection based on Bateman's principles.

Despite high levels of paternal care in substrate brooding fishes, sexual selection tends to act more strongly on males than on females, which suggests that maternal investment is higher than paternal investment and that parental care does not limit the reproductive rate for males. In pumpkinseed sunfish, selection favors parents with high levels of defense that may exclude predators more effectively and, as suggested by Bateman's measures, alternative reproductive strategies may decrease the opportunity for sexual selection within the parental strategy. In teleost fishes with internal fertilization, patterns of parental investment and intensity of sexual selection seem to support Bateman's principles, but further studies using these systems and these measures of selection will improve the understanding of factors affecting the intensity of sexual selection and its relation to mating systems.

Since tools of molecular genetics became readily available, our understanding of bird mating systems has undergone a revolution. The majority of passerine species investigated are socially monogamous, but have been shown to be genetically polygamous. Data sets from natural populations of juncos suggest that multiple mating by females results in a sexual selection gradient as steep for females as for males (a result that does not support Bateman's predictions). However, in males, fitness is enhanced directly through fertilization success with multiple matings; in females fitness benefits may be enhanced immediately through direct access to food, protection against predators, or other resources received from males, or they may be delayed through improvement in offspring quality (e.g., through good genes, or greater genetic compatibility between the female and the extra-pair male). But a steep sexual selection gradient for females can be difficult to interpret. If all females copulate with multiple partners that are equally likely to fertilize eggs, then females that produce larger clutch sizes, for any reason, will appear to have copulated with more males. That is, multiple sires have a higher probability of detection in larger clutches than in smaller ones, giving the impression that females that mate with multiple males increase their reproductive success. Yet, in most studies in which there is a correlation between number of offspring produced by females and number of extra-pair males, causation has not been clearly established and other factors may explain the results. Additional complications in understanding male and female reproductive strategies are: (1) Molecular studies cannot detect extra-pair copulations that did not result in fertilizations; yet if a female acquires food or other resources from extra-pair males, such extra-pair matings may have significant effects on female fitness. Thus, molecular studies provide only a conservative estimate of the number of extra-pair copulations or “mates” that a female has. (2) Clutch size affects the probability that any given male will be successful in fertilizing a female's eggs. Specifically, at any given point, a male's chances of fertilizing at least one egg in the female's clutch will be greater as clutch size increases. We predict that in avian species with small clutch sizes, males may be selected to be choosy and avoid extra-pair copulations, while females should be selected to be less discriminating. Moreover, if extra-pair males provide resources that increase female fitness, the females should seek extra-pair copulations, whether or not the males are likely to fertilize any of her eggs.

Laboratory studies with insects have yielded clearer evidence of the causal relationship between multiple mating and increased female fitness. We review studies on a tenebrionid beetle in which female fecundity increases directly with number of mates. In these experiments, the nutritive value of the spermatophores does not fully explain the increase in female reproductive success.

The sex-specific slopes of Bateman's gradients have important implications for understanding animal mating systems, including patterns of sexual selection and reproductive competition. Intersexual differences in the fitness benefits derived from mating with multiple partners are expected to yield distinct patterns of reproductive success for males and females, with variance in direct fitness predicted to be greater among males. These analyses assume that typically all adults are reproductive and that failure to produce offspring is non-adaptive. Among some species of cooperatively breeding birds and mammals, however, non-breeding adult alloparents are common and may comprise the majority of individuals in social groups. The presence of a large number of non-breeding adults, particularly when coupled with greater social suppression of reproduction among females, may alter the relative variance in direct fitness between the sexes, thereby generating an apparent contradiction to Bateman's Paradigm. To explore quantitatively the effects of non-breeding alloparents on variance in reproductive success, we used genetic estimates of parentage and reproductive success drawn from the literature to calculate the relative variability in direct fitness for females and males in alloparental and “other” societies of birds and mammals. Our analyses indicate that in mammals and, to a lesser extent, in birds, variability in direct fitness is greater among females in species characterized by the presence of non-breeding alloparents. These data suggest that social interactions, including social suppression of reproduction, are powerful determinants of individual direct fitness that may modify sex-specific patterns of reproductive variance from those described by Bateman.

The breeding system of an animal population is thought to depend on the ability of one sex (usually the male) to acquire mates, either directly through association with females or indirectly through defense of the resources desired by females. The sex that contributes most to infant care (usually the female) is constrained by parental involvement and thereby limits reproduction of the opposite sex. Accordingly, males, but not females, enhance their reproductive success by acquiring additional mates. This classical view has emphasized the role of male–male competition in sexual selection, at the expense of fully exploring the potential for female choice. A more recent shift in focus has revealed substantial variation in female reproductive success and increasingly accentuates the importance of female intrasexual competition and male mate choice. A comparative review of primate reproduction, therefore, challenges expectations of male control and female compliance, and calls for a comprehensive treatment of costs and benefits that extends beyond conventional mention of heavy female investment versus male negligence or absenteeism. For individuals that manipulate their social environment or reproductive output, consideration of more subtle, even cryptic, aspects of female behavior and physiology (e.g., social strategizing, sexual solicitation or rejection, sexual advertisement or concealed ovulation, multiple mating, and reproductive failure) raises the question of whether females can be effectively ‘monopolized.’ Widespread patterns that counter Bateman's paradigm call for a reexamination of the predictions generated by dichotomizing gametes into ‘expensive eggs’ and ‘cheap sperm,’ and encourage continued mechanistic research focused on conception quality rather than quantity.

The widespread use of molecular markers to estimate parentage makes possible a new index of the opportunity for sexual selection. After demonstrating the need for a new measure, I develop one based on the upper limit on sexual selection. I describe what sets the upper limit for each sex by showing how maximum fecundity increases with number of mates, accounting for the amount of energy (or critical resources) available for reproduction and levels of parental care. For females the upper limit on sexual selection is set by the value of paternal investment that comes with each mating. For males, the upper limit on sexual selection is set by the fecundity of their mates (including any boost to female fecundity from paternal investment). Sex-roles are most likely to reverse (making males choosy and females competitive) when the amount of reproductive energy investment made by each sex is low, irrespective of the level of paternal investment. Finally, I propose that we use the difference between male and female upper limits on sexual selection to quantify sex differences in the opportunity for sexual selection. Using upper limits to estimate the opportunity for sexual selection is more intuitive than older methods (e.g., standardized variance in mating success), it is experimentally measurable, and it is valuable in understanding the evolution of mating systems.

An alternative to classic sexual selection hypotheses for sex differentiated pre-mating behavior is that time available for mating—as individuals experience it—along with fitness differences among alternative potential mates, induces choosy versus indiscriminate mating behavior. This alternative hypothesis says that selection has acted so that all individuals flexibly express fitness-enhancing choosy, indiscriminate, and competitive mating behavior, induced by time-varying life histories, environmental and social cues. Key predictions of DYNAMATE, the formal model of adaptively flexible sex role behavior of individuals of both sexes within dynamically changing populations, include: (1) All individuals regardless of sex assess likely fitness outcomes from mating with alternative potential mates before expressing choosy or indiscriminate behavior. (2) Males and females express adaptively flexible, choosy and indiscriminate behavior so that individuals may change their behavior—from moment to moment—to fit dynamically changing circumstances. (3) Indiscriminate behavior of males and (4) choosy behavior of females would often be maladaptive even in species with greater female than male parental investment, when females have longer latencies to receptivity to re-mating than males, and when the relative reproductive rate of males is greater than in females. (5) Whether or not females show choosy behavior will not affect whether or not males exhibit choosy or indiscriminate behavior, and vice versa. (6) When other model parameters are equal, the proportion of individuals of a given sex expressing choosy or indiscriminate mating behavior is a function of the distribution of fitness ratios (a distribution of all fitness differences that would be conferred on an individual by mating with any two sequentially or simultaneously encountered alternative potential mates). (7) Whether same-sex individuals behaviorally compete is a function of the fitness that would be conferred if the strategist won access to a potential mate, but not a function of relative reproductive rate or its proxy, the operational sex ratio. We call for re-evaluation of sex differences in choosy, indiscriminate, and competitive behavior under strong experimental controls that level the ecological playing fields of males and females, i.e., under experimental conditions informing the mechanisms of phenotypic expression. We end with comments on the classic question of questions: why are the sexes as they are?

Bateman identified two aspects of sexual selection. The first, called Bateman's principle, is that sexual selection favors increased promiscuity of males but not of females as a result of differences in parental investment in gametes. The second is that the variance in mate number of males is the fundamental cause of a sex difference in fitness variance. We argue that Bateman's insight about the source of sexual selection is more fundamental than his speculation about patterns of parental investment. We show that, when the sex ratio is 1:1, the average female must be as promiscuous as the average male, because each copulation involves one male and one female. Because mean male and female promiscuity are tied together in the same manner as mean male and female fitness, a sex difference in mating propensity must be the result of either (1) a sex difference in the covariance between matings and number offspring, or (2) Fisherian run-away sexual selection, wherein female reluctance to mate is a weak form of female choice. We show how female promiscuity can limit the evolution of male promiscuity, turning the central argument of parental investment theory on its head.