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Darwin and Bateman suggested that precopulatory sexual selection is more intense on males than females, and that this difference is due to anisogamy (i.e. dimorphism in gamete size and number). While a recent paper apparently presents empirical support for this hypothesis, another appears at first sight to present evidence against it. We argue that this is partly due to lack of transparent theoretical predictions, and discuss and analyze sexual selection theory in relation to anisogamy evolution. On one hand, we find that there exists relatively little theory that can directly address all the tested predictions; on the other, the picture painted by current theory indicates that both sets of empirical results broadly match predictions about the causal link between anisogamy and sexual selection, thus reconciling the two apparently opposing claims. We also discuss in a very broad, general sense how anisogamy is expected to affect sexual selection. [ABSTRACT FROM AUTHOR]

The article discusses the impact of population size, structure, fertilization success, and propagule dimorphism on sex allocation in simultaneous hermaphrodites, focusing on plant reproduction. The authors present a mathematical model that challenges classical sex allocation theory by showing that population size, pollen mortality, and fertilization success can influence sex allocation. The study reanalyzes the model and confirms the classical result of equal sex allocation under panmixia. The research highlights the importance of considering population structure and dispersal rates in understanding sex allocation evolution. [Extracted from the article]

The origin and maintenance of sex differences in reproductive behavior (often labeled sex roles) have remained controversial topics, and recent meta-analyses and theoretical models have helped to elucidate the processes that generate diverse sex roles. We are glad to see that our study (Mokos et al. 2021) generated a healthy debate, and in agreement with recent commentaries (Janicke, 2024 ; Lehtonen & Parker, 2024) we call for a more comprehensive approach to understanding sex role evolution. [ABSTRACT FROM AUTHOR]

Sexual selection is both widely studied and widely debated. We assess a central but criticised aspect of sexual selection theory: that is, the claim of a causal effect from gamete dimorphism to the evolution of sex differences. Although a small number of recent models have explicitly analysed the causal link from gamete dimorphism to sexual selection, we find that the majority of models in sexual selection do not do so. Critical questions and debates force researchers to look deeper into the foundations of theory, and to find ways to develop theory that bridges gaps in existing research. Such research can be complementary to classical theory and stand alongside it, rather than replace it. Sexual selection is a field coloured by tension and contrasting views. One contested claim is the causal link from the definition of the sexes (anisogamy) to divergent selection on the sexes. Does theory truly engage with this claim? We survey the extent to which theory makes sex-specific assumptions and engages with anisogamy, and discuss these issues in a broader context. The majority of theory in sexual selection makes sex-specific assumptions and does not engage with the definition of the sexes. While this does not invalidate existing results, debates and criticisms regarding sexual selection force us to think deeper about its logical foundations. We discuss ways to strengthen the foundations of sexual selection theory by relaxing central assumptions. [ABSTRACT FROM AUTHOR]

Anisogamy—the size dimorphism of gametes—is the defining difference between the male and female sexual strategies. Game-theoretic thinking led to the first convincing explanation for the evolutionary origins of anisogamy in the 1970s. Since then, formal game-theoretic models have continued to refine our understanding of when and why anisogamy should evolve. Such models typically presume that the earliest anisogamous organisms had separate sexes. However, in most taxa, there is no empirical evidence to support this assumption. Here, we present a model of the coevolution of gamete size and sex allocation, which allows for anisogamy to emerge alongside either hermaphroditism or separate sexes. We show that hermaphroditic anisogamy can evolve directly from isogamous ancestors when the average size of spawning groups is small and fertilization is relatively efficient. Sex allocation under hermaphroditism becomes increasingly female-biased as group size decreases and the degree of anisogamy increases. When spawning groups are very small, our model also predicts the existence of complex isogamous organisms in which individuals allocate resources equally to two large gamete types. We discuss common, but potentially unwarranted, assumptions in the literature that could be relaxed in future models. This article is part of the theme issue 'Half a century of evolutionary games: a synthesis of theory, application and future directions'. [ABSTRACT FROM AUTHOR]

What is it for an animal to be female, or male? An emerging consensus among philosophers of biology is that sex is grounded in some manner or another on anisogamy, that is, the ability to produce either large gametes (egg) or small gametes (sperm), though the exact nature of this grounding remains contentious. Here we argue for a new conception of this relation. In our view, one’s sex doesn’t depend on the kind of gamete one is capable of making, but on the kind of gamete one is designed to make, where design is understood in terms of an evolutionary or ontogenetic selection process. Specifically, we argue that what it is to be, say, male, is to have a part or process that has the (proximal or distal) biological function of producing sperm. We outline and defend our view, and sketch some implications for scientific and social problems related to sex. [ABSTRACT FROM AUTHOR]

The evolution of gametic sex (meiosis and fertilization) and subsequent transition from isogamy (fusion between two equal-sized gametes) to anisogamy (dimorphism into eggs and sperm, namely, females and males) is one of the largest enigmas of evolutionary biology. Meiosis entails genome-dilution cost and anisogamy entails male-production cost. Despite much progress has been made for the maintenance mechanisms of sex, its origination events under such "twofold cost of sex" are still unsolved. Here, we posit two hypothetical scenarios as follows: the "Seesaw Effect" hypothesizes that automictic selfing between isogametes effectively purged deleterious mutations from an organism's lineage and simultaneously fixed the sex-controlling allele and all other loci (no genome-dilution cost raised). The high relatedness among homoeologous cell colonies led to multicellularization. The "inflated isogamy" hypothesizes that multicellularity increased the reproductive investment of both mates, resulting in excessively large isogametes. This redundancy induced cheating of one sex (evolving to male) to reduce gamete size. However, the other sex (evolving to female) allowed this cheat because her cost did not change. Therefore, anisogamy originated as a kind of commensalism but turned into beneficial for females because it solved the gamete limitation problem inherent to isogamy. Thus, smooth transition to anisogamy had been attained. [ABSTRACT FROM AUTHOR]

In eukaryotes, gamete size difference between the two sexes (anisogamy) evolved from gametes of equal size in both mating types (isogamy). The gamete dynamics (GD) model for anisogamy evolution combines gamete limitation and competition and predicts that if gametes of both mating types can develop parthenogenetically (i.e. without fusing with the opposite mating type), large isogamy can evolve under gamete-limited conditions. Ulvophycean marine green algae that have been claimed to exhibit various gametic systems from isogamy to anisogamy are important models for testing such theories. However, in most previous papers, whether a species is isogamous or anisogamous has not been examined statistically. Caution is necessary regarding claims of slight anisogamy because of gamete size variation. We reveal (i) that the gametic system of Struvea okamurae is large isogamy using a generalized linear mixed model, which accounted for the variation of gamete size among individual gametophytes, and (ii) that gametes of this alga can actually develop parthenogenetically, contrary to a previous report. Its habitat environments and protracted duration of gamete release suggest that this alga might experience gamete-limited conditions. Struvea okamurae seems to produce large parthenogenetic isogametes following GD model predictions, as an adaptation to deep waters.

The two sexes are defined by the sizes of the gametes they produce, anisogamy being the state with two differing gamete sizes (hence, females and males). The origin of this divergence has received much research interest, both theoretically and empirically. The gamete dynamics (GD) theory is a widely accepted theoretical explanation for anisogamy, and green algae have been an important empirical testing ground for the theory. However, some green and brown algae produce parthenogenetic gametes (gametes that can develop without fusing with another gamete), in contrast to an assumption in GD theory that unfused gametes do not develop. Here, we construct a GD model accounting for parthenogenetic gametes. We find that under conditions of panmixia and highly efficient fertilization (i.e., conditions of classical GD models from 1972 onward), the results remain largely unaltered by parthenogametes. However, under gamete-limited conditions anisogamy evolves less easily in the new model, and a novel result emerges: whereas previous models typically predict the evolution of either anisogamy or small isogamy, the current model shows that large isogamy can evolve when parthenogenetic gametes evolve under conditions of inefficient fertilization. Our analyses uncover unexplored complications relating to sex ratios under this relatively uncharted gametic system. We discuss limitations these complications impose on our models and suggest avenues for future research. We compare model results to algae with parthenogenetic gametes in nature. [ABSTRACT FROM AUTHOR]

The gametes of chlorophytes can be divided into two morphological types (types α and β) based on the position of the mating structure relative to the flagella and eyespot. To elucidate the relationship between the morphological types and the sexes, we studied spatial relationships between the flagellar apparatus‐eyespot‐mating structures in biflagellate male and female gametes and their fate after fertilization in the anisogamous (Monostroma angicava) and the slightly anisogamous species (Collinsiella cava) using field emission scanning electron microscopy and transmission electron microscopy. The smaller male and larger female gametes of M. angicava had two basal bodies arranged at a 180° angle and the cell surface coated with square‐shaped body scales, except for the flagella and mating structures. The mating structure of the female gamete was located on the same side of the flagellar beat plane as the eyespot (type β), whereas that of the male gamete was located on the opposite side (type α). This mating structure arrangement was also confirmed in C. cava. The initial fusion when male and female gametes were mixed involved the mating structures. In a fusing pair of gametes, each flagellum of one gamete lay alongside one flagellum of the other gamete. As fusion proceeded, the gamete pair transformed into a quadriflagellate planozygote, in which the four basal bodies were arranged in a cruciate pattern. The eyespots were positioned side‐by‐side on the same side of the cell. These results suggest that the two morphological types of gametes are intimately correlated with the particular sexes. [ABSTRACT FROM AUTHOR]

Decades of research on sexual selection have demonstrated that ‘conventional’ Darwinian sex roles are common in species with anisogamous gametes, with those species often exhibiting male-biased sexual selection. Yet, mating system characteristics such as long-term sperm storage and polyandry have the capacity to disrupt this pattern. Here, these ideas were explored by quantifying sexual selection metrics for the western diamond-backed rattlesnake (Crotalus atrox). A significant standardized sexual selection gradient was not found for males (βSS = 0.588, p = 0.199) or females (βSS = 0.151, p = 0.664), and opportunities for sexual selection (Is) and selection (I) did not differ between males (Is = 0.069, I = 0.360) and females (Is = 0.284, I = 0.424; both p > 0.05). Furthermore, the sexes did not differ in the maximum intensity of precopulatory sexual selection (males: s′max = 0.155, females: s′max = 0.080; p > 0.05). Finally, there was no evidence that male snout–vent length, a trait associated with mating advantage, is a target of sexual selection (p > 0.05). These results suggest a lack of male-biased sexual selection in this population. Mating system characteristics that could erode male-biased sexual selection, despite the presence of conventional Darwinian sex roles, are discussed.

Based on the morphology of gametes, sexual reproduction in brown algae is usually classified into three types: isogamy, anisogamy, and oogamy. In isogamy, chloroplasts and chloroplast DNA (chlDNA) in the sporophyte cells are inherited biparentally, while mitochondria (or mitochondrial DNA, mtDNA) is inherited maternally. In oogamy, chloroplasts and mitochondria are inherited maternally. However, the patterns of mitochondrial and chloroplast inheritance in anisogamy have not been clarified. Here, we examined derivation of mtDNA and chlDNA in the zygotes through strain-specific PCR analysis using primers based on single nucleotide polymorphism in the anisogamous brown alga Mutimo cylindricus. In 20-day-old sporophytes after fertilization, mtDNA and chlDNA derived from female gametes were detected, thus confirming the maternal inheritance of both organelles. Additionally, the behavior of mitochondria and chloroplasts in the zygotes was analyzed by examining the consecutive serial sections using transmission electron microscopy. Male mitochondria were isolated or compartmentalized by a double-membrane and then completely digested into a multivesicular structure 2 h after fertilization. Meanwhile, male chloroplasts with eyespots were observed even in 4-day-old, seven-celled sporophytes. The final fate of male chloroplasts could not be traced. Organelle DNA copy number was also examined in female and male gametes. The DNA copy number per chloroplast and mitochondria in male gametes was lower compared with female organelles. The degree of difference is bigger in mtDNA. Thus, changes in different morphology and DNA amount indicate that maternal inheritance of mitochondria and chloroplasts in this species may be based on different processes and timing after fertilization. [ABSTRACT FROM AUTHOR]

The past half century has seen the development of the field of post-ejaculatory sexual selection, the sequel to sexual selection for mateacquisition (pre-ejaculatory) described by Darwin. In richness and diversity of adaptations, post-ejaculatory selection rivals that of pre-ejaculatory sexual selection. Anisogamy--and hence two sexes--likely arose by primeval gamete competition, and sperm competition remains a major force maintaining high sperm numbers. The post-ejaculatory equivalent of male-male competition for matings, sperm competition was an intense ancestral form of sexual selection, typically weakening as mobility and internal fertilization developed in many taxa, when some expenditure became diverted into pre-ejaculatory competition. Sperm competition theory has been relatively successful in explaining variation in relative testes size and sperm numbers per ejaculate and is becoming more successful in explaining variation in sperm phenotype. Sperm competition has generated many other male adaptations such as seminal fluid proteins that variously modify female reproduction towards male interests, and copulatory plugs, prolonged copulations and post-ejaculatory guarding behaviour that reduce female remating probability, many of which result in sexual conflict. This short survey of conceptual developments is intended as a broad overview, mainly as a primer for new researchers. [ABSTRACT FROM AUTHOR]

• The validity of Bateman principles remains an ongoing debate among biologists. • Bateman's views on sex roles are deeply enmeshed with sex stereotypes and anisogamy. • Bateman's gradients are often considered useful metrics, confirmed by field studies. • But Bateman's gradients also seem to be impossible to refute. [ABSTRACT FROM AUTHOR]

Colonies of insects such as ants and honeybees are commonly viewed as 'superorganisms', with division of labour between reproductive 'germline-like' queens and males and 'somatic' workers. On this view, properties of the superorganismal colony are comparable with those of solitary organisms to such an extent that the colony itself can be viewed as a unit analogous to an organism. Thus, the concept of a superorganism can be useful as a guide to thinking about life history and allocation traits of colonies as a whole. A pattern that seems to reoccur in insects with superorganismal societies is size dimorphism between queens and males, where queens tend to be larger than males. It has been proposed that this is analogous to the phenomenon of anisogamy at the level of gametes in organisms with separate sexes; more specifically, it is suggested that this caste dimorphism may have evolved via similar selection pressures as gamete dimorphism arises in the 'gamete competition' theory for the evolution of anisogamy. In this analogy, queens are analogous to female gametes, males are analogous to male gametes, and colony survival is analogous to zygote survival in gamete competition theory. Here, we explore if this question can be taken beyond an analogy, and whether a mathematical model at the superorganism level, analogous to gamete competition at the organism level, may explain the caste dimorphism seen in superorganismal insects. We find that the central theoretical idea holds, but that there are also significant differences between the way this generalized 'propagule competition' theory operates at the levels of solitary organisms and superorganisms. In particular, we find that the theory can explain superorganismal caste dimorphism, but compared with anisogamy evolution, a central coevolutionary link is broken, making the requirements for the theory to work less stringent than those found for the evolution of anisogamy. [ABSTRACT FROM AUTHOR]

We reexamine the influential parental investment hypothesis proposed by Trivers for the causal relationship between anisogamy and widespread female‐biased parental care. We build self‐consistent versions of Maynard Smith's simple evolutionary game between males and females over parental care, and incorporate consequences of anisogamy for gamete production and its trade‐off with parental care, and for patterns of mate limitation. As male mating opportunities are limited by females, frequency‐dependent selection acts on male strategies. Assuming synchrony of matings in the population, our analytical models find either symmetric sex roles or male‐biased care as an evolutionarily stable strategy (ESS), in contrast to Trivers' hypothesis. We simulate evolution in asynchronously mating populations and find that diverse parental roles, including female care, can be ESS depending on the parameters. When caring males can also remate, or when females can increase the clutch size by deserting, there is stronger selection for male‐biased care. Hence, we argue that the mating‐caring trade‐off for males is neither a necessary consequence of anisogamy nor sufficient to select for female‐biased care. Instead, the factors excluded from our models—costly competitive traits, sexual selection, and partial parentage—may be necessary for the parental investment hypothesis to work. [ABSTRACT FROM AUTHOR]

In 1948, British geneticist A. J. Bateman published in the journal Heredity the results of his experiments on the fruit fly Drosophila melanogaster. Bateman hoped he was bringing evidence for the 'greater dependence of males for their fertility on frequency of insemination' (Bateman, 1948, Heredity, 2 (3), p. 364), thus purportedly explaining 'an undiscriminating eagerness in the males and a discriminating passivity in the females' (p. 365). At first rather neglected, Bateman's results were increasingly cited in the 1970s, especially as Bateman had suggested that what he had discovered in Drosophila could also be applied to humans. However, throughout the years, criticisms of the paper accumulated to the point that biologists are now divided into two groups: those who praise Bateman as one of the founding fathers of the discipline of behavioural ecology, and those who claim his paper was fatally flawed. The present paper follows the 'strange fate' of Bateman's article: initially barely cited, the paper was 'rediscovered' by Robert Trivers in 1972 (Trivers, 1972, Parental investment and sexual selection. In B. G. Campbell (Ed.), Sexual selection and the descent of man: The Darwinian pivot , pp. 136–179, New Brunswick, NJ: Transaction Publishers) and finally, the paper received numerous scathing critiques in more recent years, on a methodological and empirical basis. • Bateman's (1948) paper reached 'paradigm' status before being highly criticized. • Supporters and critics of Bateman are equally passionate in their evaluations. • Citations of Bateman (1948) have not declined despite failed attempts at replication. • Bateman (1948) is a classic case study for the Kuhnian epistemology of paradigms. [ABSTRACT FROM AUTHOR]

Abstract The disruptive selection theory of the evolution of anisogamy posits that the evolution of a larger body or greater organismal complexity selects for a larger zygote, which in turn selects for larger gametes. This may provide the opportunity for one mating type to produce more numerous, small gametes, forcing the other mating type to produce fewer, large gametes. Predictions common to this and related theories have been partially upheld. Here, a prediction specific to the disruptive selection theory is derived from a previously published game‐theoretic model that represents the most complete description of the theory. The prediction, that the ratio of macrogamete to microgamete size should be above three for anisogamous species, is supported for the volvocine algae. A fully population genetic implementation of the model, involving mutation, genetic drift, and selection, is used to verify the game‐theoretic approach and accurately simulates the evolution of gamete sizes in anisogamous species. This model was extended to include a locus for gamete motility and shows that oogamy should evolve whenever there is costly motility. The classic twofold cost of sex may be derived from the fitness functions of these models, showing that this cost is ultimately due to genetic conflict.

Recently, it was pointed out that classic models for the evolution of anisogamy do not take into account the possibility of parthenogenetic reproduction, even though sex is facultative in many relevant taxa (e.g., algae) that harbour both anisogamous and isogamous species. Here, we complement this recent analysis with an approach where we assume that the relationship between progeny size and its survival may differ between parthenogenetically and sexually produced progeny, favouring either the former or the latter. We show that previous findings that parthenogenesis can stabilise isogamy relative to the obligate sex case, extend to our scenarios. We additionally investigate two different ways for one mating type to take over the entire population. First, parthenogenesis can lead to biased sex ratios that are sufficiently extreme that one type can displace the other, leading to de facto asexuality for the remaining type that now lacks partners to fuse with. This process involves positive feedback: microgametes, being numerous, lack opportunities for syngamy, and should they proliferate parthenogenetically, the next generation makes this asexual route even more prominent for microgametes. Second, we consider mutations to strict asexuality in producers of micro- or macrogametes, and show that the prospects of asexual invasion depend strongly on the mating type in which the mutation arises. Perhaps most interestingly, we also find scenarios in which parthenogens have an intrinsic survival advantage yet facultatively sexual isogamous populations are robust to the invasion of asexuals, despite us assuming no genetic benefits of recombination. Here, equal contribution from both mating types to zygotes that are sufficiently well provisioned can outweigh the additional costs associated with syngamy.

Females are expected to have evolved to be more discriminatory in mate choice than males as a result of greater reproductive investment into larger gametes (eggs vs. sperm). In turn, males are predicted to be more promiscuous than females, showing both a larger variance in the number of mates and a greater increase in reproductive success with more mates, yielding more intense sexual selection on males vs. females (Bateman's Paradigm). However, sex differences in costly parental care strategies can either reinforce or counteract the initial asymmetry in reproductive investment, which may be one cause for some studies failing to conform with predictions of Bateman's Paradigm. For example, in many bird species with small female‐biased initial investment but extensive biparental care, both sexes should be subject to similar strengths of sexual selection because males and females are similarly restricted in their ability to pursue additional mates. Unlike 99% of avian species, however, obligate brood parasitic birds lack any parental care in either sex, predicting a conformation to Bateman's Paradigm. Here we use microsatellite genotyping to demonstrate that in brood parasitic brown‐headed cowbirds (Molothrus ater), per capita annual reproductive success increases with the number of mates in males, but not in females. Furthermore, also as predicted, the variance of the number of mates and offspring is greater in males than in females. Thus, contrary to previous findings in this species, our results conform to predictions of the Bateman's Paradigm for taxa without parental care. [ABSTRACT FROM AUTHOR]

Transition from isogamy to anisogamy, hence males and females, leads to sexual selection, sexual conflict, sexual dimorphism, and sex roles. Gamete dynamics theory links biophysics of gamete limitation, gamete competition, and resource requirements for zygote survival and assumes broadcast spawning. It makes testable predictions, but most comparative tests use volvocine algae, which feature internal fertilization. We broaden this theory by comparing broadcast-spawning predictions with two plausible internal-fertilization scenarios: gamete casting/brooding (one mating type retains gametes internally, the other broadcasts them) and packet casting/brooding (one type retains gametes internally, the other broadcasts packets containing gametes, which are released for fertilization). Models show that predictions are remarkably robust to these radical changes, yielding (1) isogamy under low gamete limitation, low gamete competition, and similar required resources for gametes and zygotes, (2) anisogamy when gamete competition and/or limitation are higher and when zygotes require more resources than gametes, as is likely as multicellularity develops, (3) a positive correlation between multicellular complexity and anisogamy ratio, and (4) under gamete competition, only brooders becoming female. Thus, gamete dynamics theory represents a potent rationale for isogamy/anisogamy and makes similar testable predictions for broadcast spawners and internal fertilizers, regardless of whether anisogamy or internal fertilization evolved first. [ABSTRACT FROM AUTHOR]

The evolution of anisogamy or gamete size dimorphism is a fundamental transition in evolutionary history, and it is the origin of the female and male sexes. Although mathematical models attempting to explain this transition have been published as early as 1932, the 1972 model of Parker, Baker, and Smith is considered to be the first explanation for the evolution of anisogamy that is consistent with modern evolutionary theory. The central idea of the model is ingenious in its simplicity: selection simultaneously favours large gametes for zygote provisioning, and small gametes for numerical competition, and under certain conditions the outcome is anisogamy. In this article, I derive novel analytical solutions to a 2002 game theoretical update of the 1972 anisogamy model, and use these solutions to examine its robustness to variation in its central assumptions. Combining new results with those from earlier papers, I find that the model is quite robust to variation in its central components. This kind of robustness is crucially important in a model for an early evolutionary transition where we may only have an approximate understanding of constraints that the different parts of the model must obey.

Although the gamete competition theory remains the dominant explanation for the evolution of anisogamy, well-known exceptions to its predictions have raised doubts about the completeness of the theory. One of these exceptions is isogamy in large or complex species of green algae. Here, we show that this exception may be explained in a manner consistent with a gametheoretic extension of the original theory: a constraint on the minimum size of a gamete may prevent the evolution of continuously stable anisogamy. We show that in the volvocine algae, both gametes of isogamous species retain an intact chloroplast, whereas the chloroplast of the microgamete in anisogamous species is invariably degenerate. The chloroplast, which functions in photosynthesis and starch storage, may be necessary to provision a gamete for an extended period when gamete encounter rates are low. The single chloroplast accounts for most of the volume of a typical gamete, and thus may constrain the minimum size of a gamete, preventing the evolution of anisogamy. A prediction from this hypothesis, that isogametes should be larger than the microgametes of similar-size species, is confirmed for the volvocine algae. Our results support the gamete competition theory. [ABSTRACT FROM AUTHOR]

Computer experiments that mirror the evolutionary dynamics of sexual and asexual organisms as they occur in nature were used to test features proposed to explain the evolution of sexual recombination. Results show that this evolution is better described as a network of interactions between possible sexual forms, including diploidy, thelytoky, facultative sex, assortation, bisexuality, and division of labor between the sexes, rather than a simple transition from parthenogenesis to sexual recombination. Diploidy was shown to be fundamental for the evolution of sex; bisexual reproduction emerged only among anisogamic diploids with a synergistic division of reproductive labor; and facultative sex was more likely to evolve among haploids practicing assortative mating. Looking at the evolution of sex as a complex system through individual-based simulations explains better the diversity of sexual strategies known to exist in nature, compared to classical analytical models. [ABSTRACT FROM AUTHOR]

From the male peacock's tail plumage to the floral displays of flowering plants, traits related to sexual reproduction are often complex and exaggerated. Why has sexual reproduction become so complicated? Why have such exaggerated sexual traits evolved? Early work posited a connection between multicellularity and sexual traits such as anisogamy (i.e., the evolution of small sperm and large eggs). Anisogamy then drives the evolution of other forms of sexual dimorphism. Yet the relationship between multicellularity and the evolution of sexual traits has not been empirically tested. Given their extensive variation in both multicellular complexity and sexual systems, the volvocine green algae offer a tractable system for understanding the interrelationship of multicellular complexity and sex. Here we show that species with greater multicellular complexity have a significantly larger number of derived sexual traits, including anisogamy, internal fertilization, and secondary sexual dimorphism. Our results demonstrate that anisogamy repeatedly evolved from isogamous multicellular ancestors and that anisogamous species are larger and produce larger zygotes than isogamous species. In the volvocine algae, the evolution of multicellularity likely drives the evolution of anisogamy, and anisogamy subsequently drives secondary sexual dimorphism. Multicellularity may set the stage for the overall diversity of sexual complexity throughout the Tree of Life. [ABSTRACT FROM AUTHOR]

Summary: Patterns of species richness are commonly linked to life history strategies. In diatoms, an exceptionally diverse lineage of photosynthetic heterokonts important for global photosynthesis and burial of atmospheric carbon, lineages with different locomotory and reproductive traits differ dramatically in species richness, but any potential association between life history strategy and diversification has not been tested in a phylogenetic framework. We constructed a time‐calibrated, 11‐gene, 1151‐taxon phylogeny of diatoms – the most inclusive diatom species tree to date. We used this phylogeny, together with a comprehensive inventory of first–last occurrences of Cenozoic fossil diatoms, to estimate ranges of expected species richness, diversification and its variation through time and across lineages. Diversification rates varied with life history traits. Although anisogamous lineages diversified faster than oogamous ones, this increase was restricted to a nested clade with active motility in the vegetative cells. We propose that the evolution of motility in vegetative cells, following an earlier transition from oogamy to anisogamy, facilitated outcrossing and improved utilization of habitat complexity, ultimately leading to enhanced opportunity for adaptive divergence across a variety of novel habitats. Together, these contributed to a species radiation that gave rise to the majority of present‐day diatom diversity. [ABSTRACT FROM AUTHOR]

Key message: Within-clutch gamete size variability inMonostroma angicava.Abstract: In many organisms, it is unclear how the size variation in gametes is generated in each clutch (i.e., total gametes produced by a gametophyte for a single spawning) or how gamete size is adjusted. Within-clutch variation in gamete size has been explained as a result of either physiological/developmental constraints or bet hedging during gametogenesis. These two explanations have been assumed to be mutually exclusive, and related observations are conflicting. The slightly anisogamous dioecious green alga Monostroma angicava employs a simple mechanism to produce gametes of each sex: each vegetative cell becomes a single gametangium cell, which synchronously divides to form equally sized gametes. The number of such cell divisions has several variations, which might vary gamete size. We measured the volume of gametangia in each clutch, counted the number of cell divisions in each gametangium and estimated the size of the gametes. We found that larger gametangia divided more times than smaller gametangia in both sexes, although male gametangia were smaller than female gametangia when they underwent the same number of cell divisions. Therefore, the variation in the number of cell divisions during gametogenesis serves to adjust gamete size in each sex rather than to vary it. Within-clutch gamete size variability originates in within-clutch variation in gametangium size: any factors that increase the variation in the size of gametangia can increase the within-clutch variation in gamete size. [ABSTRACT FROM AUTHOR]

Abstract: It is commonly held that differences in gametes of the two sexes (anisogamy) evolved from ancestors whose gametes were similar in size and behavior (isogamy). Underlying many hypotheses explaining anisogamy are assumed relationships between cell size and speed in the ancestral isogamous population. Using the isogamous alga Chlamydomonas reinhardtii, we explored size–speed distributions in vegetative and gamete cells of 10 cell lines, and clonal data from within two cell lines. We applied an independent speed selection approach to gamete populations of C. reinhardtii, monitoring correlated responses in size following selection for high speed. We demonstrate positive size–speed relationships in clones, cell lines, and artificially selected speed selection lines. We found different size–speed relationships in the two cell types of C. reinhardtii even though they overlap in size, suggesting that cell composition and/or programs of gene expression are capable of altering this relationship, and that the relationship is evolvable. The positive genetic size‐speed correlation means that the division of parent vegetative cells into numerous gametes trades off against not only size, but also speed, a trade‐off that has not received previous attention. Our results support reevaluating the role of speed selection in the evolution of anisogamy. [ABSTRACT FROM AUTHOR]

Abstract: Objective: The socioecological model (SEM) is a popular collection of controversial models purporting to explain mating systems in terms of ecological and social parameters. Despite its guise of objectivity, several of its hypotheses assume Victorian gender stereotypes of active, competing males heedlessly sowing their seeds, and cautious, passive females, imprisoned by greater costs of reproduction and their consequent resourceߚdependence. Methods: We enter this debate by taking a previously neglected explanatory approach borrowed from species theory. According to the Recognition Concept of sexual species, the unit of reproductive success/fitness is irreducible to fewer than two integrated subparts (minimally a male and a female). Phyletic changes in mating systems logically effect changes in fertilization systems, leading to reproductive isolation. We take our primary assumption of the average equivalence of female and male contributions to successful reproduction from the writings of the natural philosopher, Antoinette Blackwell. Results: We revisit the SEM with its contradictions and extrapolations, and develop a genderߚneutral alternative hypothesis termed SpecificߚMate Contact (SMC), centered on two fundamental mating strategies: sexual animals may behave as synchronous mateߚattractors or asynchronous mateߚseekers, generating four possible mating system combinations (monogamy: two attractors; promiscuity: two seekers; polygyny: male attractor and female seeker; polyandry: female attractor and male seeker). Conclusions: Our approach predicts all known primate mating systems using a neutral (nonߚsexist) principle. The approach is also neutral in the sense that it does not invoke either competition or cooperation: fertilization success is considered a posteriori and males and females are coߚadapted to this end rather than cognitively cooperative. [ABSTRACT FROM AUTHOR]

The disruptive selection theory of the evolution of anisogamy posits that the evolution of a larger body or greater organismal complexity selects for a larger zygote, which in turn selects for larger gametes. This may provide the opportunity for one mating type to produce more numerous, small gametes, forcing the other mating type to produce fewer, large gametes. Predictions common to this and related theories have been partially upheld. Here, a prediction specific to the disruptive selection theory is derived from a previously published game-theoretic model that represents the most complete description of the theory. The prediction, that the ratio of macrogamete to microgamete size should be above three for anisogamous species, is supported for the volvocine algae. A fully population genetic implementation of the model, involving mutation, genetic drift, and selection, is used to verify the game-theoretic approach and accurately simulates the evolution of gamete sizes in anisogamous species. This model was extended to include a locus for gamete motility and shows that oogamy should evolve whenever there is costly motility. The classic twofold cost of sex may be derived from the fitness functions of these models, showing that this cost is ultimately due to genetic conflict. [ABSTRACT FROM AUTHOR]

The term 'sex roles' encapsulates male-female differences in mate searching, competitive traits that increase mating/fertilization opportunities, choosiness about mates and parental care. Theoretical models suggest that biased sex ratios drive the evolution of sex roles. To model sex role evolution, it is essential to note that in most sexually reproducing species (haplodiploid insects are an exception), each offspring has one father and one mother. Consequently, the total number of offspring produced by each sex is identical, so the mean number of offspring produced by individuals of each sex depends on the sex ratio (Fisher condition). Similarly, the total number of heterosexual matings is identical for each sex. On average, neither sex can mate nor breed more often when the sex ratio is even. But equally common in which sex ratio? The Fisher condition only applies to some reproductive measures (e.g. lifetime offspring production or matings) for certain sex ratios (e.g. operational or adult sex ratio; OSR, ASR). Here, we review recent models that clarify whether a biased OSR, ASR or sex ratio at maturation (MSR) have a causal or correlational relationship with the evolution of sex differences in parental care and competitive traits--two key components of sex roles. We suggest that it is more fruitful to understand the combined effect of the MSR and mortality rates while caring and competing than that of the ASR itself. In short, we argue that the ASR does not have a causal role in the evolution of parental care. We point out, however, that the ASR can be a cue for adaptive phenotypic plasticity in how each sex invests in parental care. [ABSTRACT FROM AUTHOR]

ABSTRACT The primitive land plant life cycle featured the production of spores of unimodal size, a condition called homospory. The evolution of bimodal size distributions with small male spores and large female spores, known as heterospory, was an innovation that occurred repeatedly in the history of land plants. The importance of desiccation-resistant spores for colonization of the land is well known, but the adaptive value of heterospory has never been well established. It was an addition to a sexual life cycle that already involved male and female gametes. Its role as a precursor to the evolution of seeds has received much attention, but this is an evolutionary consequence of heterospory that cannot explain the transition from homospory to heterospory (and the lack of evolutionary reversal from heterospory to homospory). Enforced outcrossing of gametophytes has often been mentioned in connection to heterospory, but we review the shortcomings of this argument as an explanation of the selective advantage of heterospory. Few alternative arguments concerning the selective forces favouring heterospory have been proposed, a paucity of attention that is surprising given the importance of this innovation in land plant evolution. In this review we highlight two ideas that may lead us to a better understanding of why heterospory evolved. First, models of optimal resource allocation - an approach that has been used for decades in evolutionary ecology to help understand parental investment and other life-history patterns - suggest that an evolutionary increase in spore size could reach a threshold at which small spores yielding small, sperm-producing gametophytes would return greater fitness per unit of resource investment than would large spores and bisexual gametophytes. With the advent of such microspores, megaspores would evolve under frequency-dependent selection. This argument can account for the appearance of heterospory in the Devonian, when increasingly tall and complex vegetative communities presented competitive conditions that made large spore size advantageous. Second, heterospory is analogous in many ways to anisogamy. Indeed, heterospory is a kind of re-invention of anisogamy within the context of a sporophyte-dominant land plant life cycle. The evolution of anisogamy has been the subject of important theoretical and empirical investigation. Recent work in this area suggests that mate-encounter dynamics set up selective forces that can drive the evolution of anisogamy. We suggest that similar dispersal and mating dynamics could have underlain spore size differentiation. The two approaches offer predictions that are consistent with currently available data but could be tested far more thoroughly. We hope to re-establish attention on this neglected aspect of plant evolutionary biology and suggest some paths for empirical investigation. [ABSTRACT FROM AUTHOR]

In the evolution of sexual reproduction, the development of asymmetrical gametes (anisogamy) often leads to the characterisation that males invest less in reproduction than females. This view is founded on the fact that male investment in individual gametes (sperm) and in gonadal tissue is often less than that of females. While it may be true that within a single mating interaction the relative reproductive investment by males and females differs, over their respective lifetimes an evolutionary view predicts that total lifetime reproductive investment should be the same for both sexes. We tested this prediction by measuring total reproductive investment in reproducing adult male and female seed beetles. Since seed beetle adults are facultatively aphagous, not needing to feed or drink as adults, we could track the daily loss of biomass in the reproducing adults as a proxy for total lifetime investment in maintenance and reproduction. By the end of their lifetime there was not a significant difference in total reproductive effort between males and females. Both sexes invested 70 ± 1% SE of their initial body mass in maintenance and reproduction. Altering sex ratios, creating male-biased or female-biased treatments, significantly influenced total investment between the sexes, but not in the manner predicted. Ours is one of the few studies that have measured total adult lifetime reproductive investment in an organism, and our results support the theoretical expectation of equal total reproductive investment between the sexes. [ABSTRACT FROM AUTHOR]

In eukaryotes, a fundamental phenomenon underlying sexual selection is the evolution of gamete size dimorphism between the sexes (anisogamy) from an ancestral gametic system with gametes of the same size in both mating types (isogamy). The nuclear-cytoplasmic conflict hypothesis has been one of the major theoretical hypotheses for the evolution of anisogamy. It proposes that anisogamy evolved as an adaptation for preventing nuclear-cytoplasmic conflict by minimizing male gamete size to inherit organelles uniparentally. In ulvophycean green algae, biparental inheritance of organelles is observed in isogamous species, as the hypothesis assumes. So we tested the hypothesis by examining whether cytoplasmic inheritance is biparental in Monostroma angicava , a slightly anisogamous ulvophycean that produces large male gametes. We tracked the fates of mitochondria in intraspecific crosses with PCR-RFLP markers. We confirmed that mitochondria are maternally inherited. However, paternal mitochondria enter the zygote, where their DNA can be detected for over 14 days. This indicates that uniparental inheritance is enforced by eliminating paternal mitochondrial DNA in the zygote, rather than by decreasing male gamete size to the minimum. Thus, uniparental cytoplasmic inheritance is achieved by an entirely different mechanism, and is unlikely to drive the evolution of anisogamy in ulvophyceans.

We previously showed that, across eukaryotes, universal differences do not exist between diploid females and males; hence, in the present study, we examine haploid stages. Unlike animal sperm, flowering plant sperm have nuclear pores, and so cannot be used to distinguish haploid females from males. Female and male gametes are not complementary: eggs and can fertilize eggs, whereas sperm can fertilize sperm, in some taxa. One sex of gametes is not universally parasitic on the other. Commonly held differences between eggs and sperm (e.g. only eggs, and not sperm, are large, long-lived, and immobile) do not apply to many eukaryotes. Many or all angiosperms have small eggs, sperm without flagella, and long-lived pollen. In many plants, we supposedly can distinguish females from males, although they have similar sized gametes. Theories of anisogamy are based on less energy being required to produce small sperm than large eggs. However any selective advantage of smaller sperm is nullified by sequestering most cytoplasmic biomass as residual bodies following meiosis in metazoa. Moreover, zoidogamous gymnosperms have numerous huge sperm. In both animals and plants, sperm are not the immediate products of meiosis but, instead, develop afterwards via haploid cell divisions. Consequently, we examined whether the most promising universal sexual difference in animals applies to plants and stramenopiles, namely asymmetrical female meiosis vs. symmetrical male meiosis. A few angiosperms (and some animals) have asymmetrical male meiosis, whereas many plants have symmetrical female meiosis. All bryophytes and stramenopiles with UV chromosomes do not have asymmetrical female meiosis insofar as meiosis produces two female and two male gametophytes. Homosporous monilophytes, lycophytes, and anthocerotophytes lack female vs. male meiosis, although they have distinct eggs and sperm. Therefore, currently, there are no universal criteria for distinguishing females from males across all animals, across all plants or across all stramenopiles, let alone across all eukaryotes. [ABSTRACT FROM AUTHOR]

Sperm cells provide essential, if usually diminutive, ingredients to successful sexual reproduction. Despite this conserved function, sperm competition and coevolution with female traits can drive spectacular morphological change in these cells. Here, we characterize four repeated instances of convergent evolution of sperm gigantism in Caenorhabditis nematodes using phylogenetic comparative methods on 26 species. Species at the extreme end of the 50-fold range of sperm-cell volumes across the genus have sperm capable of comprising up to 5% of egg-cell volume, representing severe attenuation of the magnitude of anisogamy. Furthermore, we uncover significant differences in mean and variance of sperm size among genotypes, between sexes, and within and between individuals of identical genotypes. We demonstrate that the developmental basis of sperm size variation, both within and between species, becomes established during an early stage of sperm development at the formation of primary spermatocytes, while subsequent meiotic divisions contribute little further sperm size variability. These findings provide first insights into the developmental determinants of inter- and intraspecific sperm size differences in Caenorhabditis. We hypothesize that life history and ecological differences among species favored the evolution of alternative sperm competition strategies toward either many smaller sperm or fewer larger sperm. [ABSTRACT FROM AUTHOR]

Darwin was the first to recognize that sexual selection is a strong evolutionary force. Exaggerated traits allow same-sex individuals to compete over access to mates and provide a mechanism by which mates are selected. It is relatively easy to appreciate how inter- and intrasexual selection work in organisms with the sensory capabilities to perceive physical or behavioural traits that signal mate quality or mate compatibility, and to assess the relative quality of competitors. It is therefore not surprising that most studies of sexual selection have focused on animals with separate sexes and obvious adaptations that function in the context of reproductive competition. Yet, many sexual organisms are both male and female at the same time, often lack sexual dimorphism and never come into direct contact at mating. How does sexual selection act in such species, and what can we learn from them? Here, we address these questions by exploring the potential for sexual selection in simultaneous hermaphrodites, sperm- and broadcast spawners, plants and fungi. Our review reveals a range of mechanisms of sexual selection, operating primarily after gametes have been released, which are common in many of these groups and also quite possibly in more familiar (internally fertilizing and sexually dimorphic) organisms. This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'. [ABSTRACT FROM AUTHOR]

Isogamy is a reproductive system where all gametes are morphologically similar, especially in terms of size. Its importance goes beyond specific cases: to this day non-anisogamous systems are common outside of multicellular animals and plants, they can be found in all eukaryotic super-groups, and anisogamous organisms appear to have isogamous ancestors. Furthermore, because maleness is synonymous with the production of small gametes, an explanation for the initial origin of males and females is synonymous with understanding the transition from isogamy to anisogamy. As we show here, this transition may also be crucial for understanding why sex itself remains common even in taxa with high costs of male production (the twofold cost of sex). The transition to anisogamy implies the origin of male and female sexes, kickstarts the subsequent evolution of sex roles, and has a major impact on the costliness of sexual reproduction. Finally, we combine some of the consequences of isogamy and anisogamy in a thought experiment on the maintenance of sexual reproduction. We ask what happens if there is a less than twofold benefit to sex (not an unlikely scenario as large short-term benefits have proved difficult to find), and argue that this could lead to a situation where lineages that evolve anisogamy--and thus the highest costs of sex--end up being associated with constraints that make invasion by asexual reproduction unlikely (the 'anisogamy gateway' hypothesis). This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'. [ABSTRACT FROM AUTHOR]

Gamete dimorphism (anisogamy) defines the sexes in most multicellular organisms. Theoretical explanations for its maintenance usually emphasize the size-related selection pressures of sperm competition and zygote survival, assuming that fertilization of all eggs precludes selection for phenotypes that enhance fertility. In external fertilizers, however, fertilization is often incomplete due to sperm limitation, and the risk of polyspermy weakens the advantage of high sperm numbers that is predicted to limit sperm size, allowing alternative selection pressures to target free-swimming sperm. We asked whether egg size and ejaculate size mediate selection on the free-swimming sperm of Galeolaria caespitosa, a marine tubeworm with external fertilization, by comparing relationships between sperm morphology and male fertility across manipulations of egg size and sperm density. Our results suggest that selection pressures exerted by these factors may aid the maintenance of anisogamy in external fertilizers by limiting the adaptive value of larger sperm in the absence of competition. In doing so, our study offers a more complete explanation for the stability of anisogamy across the range of sperm environments typical of this mating system and identifies new potential for the sexes to coevolve via mutual selection pressures exerted by gametes at fertilization. [ABSTRACT FROM AUTHOR]