Unravelling the evolution of complex reproductive traits with phenotypic engineering

The social dynamics surrounding courtship, mating and parental care are complex enough when just a single male and female are involved, but for species that employ multiple strategies for achieving fertilization success, the network of interactions among rivals, allies and suitors can be utterly complicated. Such is the case in the ocellated wrasse, Symphodus ocellatus, in which males adopt one of three mating strategies. The large, colourful “nesting males” court females, defend territories and care for fertilized eggs until they hatch. The smaller “satellite males” help the nesting males court females and guard against the third morph, the “sneaker males”, which sneak in when a nesting male is spawning with a female and surreptitiously release sperm. Sneaker males perform no courtship displays nor defend territories, so their reproductive investment is devoted entirely to sperm production. And these alternative male strategies work: 100% of nests contain some eggs fertilized by sneaker and satellite males, despite the fact that parental care is solely the responsibility of nesting males In this issue of Molecular Ecology, work to untangle the proximate mechanisms regulating the reproductive physiology of nesting males and their behaviour towards other males, which impacts the entire social network. Moreover, they describe how variation in neuroendocrine regulation can give rise to variation in reproductive traits, upon which sexual selection can act.     

Exploring the evolution of multicellularity in Saccharomyces cerevisiae under bacteria environment: An experimental phylogenetics approach

There have been over 25 independent unicellular to multicellular evolutionary transitions, which have been transformational in the complexity of life. All of these transitions likely occurred in communities numerically dominated by unicellular organisms, mostly bacteria. Hence, it is reasonable to expect that bacteria were involved in generating the ecological conditions that promoted the stability and proliferation of the first multicellular forms as protective units. In this study, we addressed this problem by analyzing the occurrence of multicellularity in an experimental phylogeny of yeasts (Sacharomyces cerevisiae) a model organism that is unicellular but can generate multicellular clusters under some conditions. We exposed a single ancestral population to periodic divergences, coevolving with a cocktail of environmental bacteria that were inoculated to the environment of the ancestor, and compared to a control (no bacteria). We quantified culturable microorganisms to the level of genera, finding up to 20 taxa (all bacteria) that competed with the yeasts during diversification. After 600 generations of coevolution, the yeasts produced two types of multicellular clusters: clonal and aggregative. Whereas clonal clusters were present in both treatments, aggregative clusters were only present under the bacteria treatment and showed significant phylogenetic signal. However, clonal clusters showed different properties if bacteria were present as follows: They were more abundant and significantly smaller than in the control. These results indicate that bacteria are important modulators of the occurrence of multicellularity, providing support to the idea that they generated the ecological conditions‐promoting multicellularity.     

Female-limited responses in remating rate and mating duration in the experimental evolution of a beetle Callosobruchus chinensis

Mating rate optima often differ between the sexes: males may increase their fitness by multiple mating, but for females multiple mating confers little benefit and can often be costly (especially in taxa without nuptial gifts or mala parental care). Sexually antagonistic evolution is thus expected in traits related to mating rates under sexual selection. This prediction has been tested by multiple studies that applied experimental evolution technique, which is a powerful tool to directly examine the evolutionary consequences of selection. Yet, the results so far only partly support the prediction. Here, we provide another example of experimental evolution of sexual selection, by applying it for the first time to the mating behaviour of a seed beetle Callsorobruchus chinensis. We found a lower remating rate in polygamy-line females than in monogamy-line (i.e. no sexual selection) females after 21 generations of selection. Polygamy-line females also showed a longer duration of first mating than monogamy-line females. We found no effect of male evolutionary lines on the remating rate or first mating duration. Though not consistent with the original prediction, the current and previous studies collectively suggest that the observed female-limited responses may be a norm, which is also consistent with the conceptual advances in the last two decades of the advantages and limitations of experimental evolution technique.     

The evolution of the development

The evolution of development required few new features not already present in the eukaryotic cell, as exemplified by the cell cycle. Moreover, the protozoa possess many features of spatial organization and regulation present in metazoan embryos.
The earliest multicellular organism could have been reproduced by a stem cell mechanism or by fission, the latter requiring cell-to-cell interactions that may have favoured cell-interactions and regulation. Regeneration can be considered as a meta-phenomenon related to asexual reproduction and retention of embryonic characters. The origin of embryonic structures like the gastrula may be accounted for in terms of Haeckel's 'Gastrea' theory. Mechanisms based on selection at the level of cell lineage are rejected.
It is not clear what selective forces act on development itself, as distinct from the requirement for reliably producing a functional orgainsm. There is, for example, a major problem why gastrulation should be so variable in related animals. Selection for rate of development in relation to energy utilization may play a role. If many variants are neutral this may facilitate the evolution of novelty.
In general terms there is a requirement for a continuity principle for the evolution of each form in development. Most groups pass through a phylotypic stage with considerable diversity before and after.     

Mating systems, sperm competition, and the evolution of sexual dimorphism in birds

Comparative analyses suggest that a variety of factors influence the evolution of sexual dimorphism in birds. We analyzed the relative importance of social mating system and sperm competition to sexual differences in plumage and body size (mass and tail and wing length) of more than 1,000 species of birds from throughout the world. In these analyses we controlled for phylogeny and a variety of ecological and life-history variables. We used testis size (corrected for total body mass) as an index of sperm competition in each species, because testis size is correlated with levels of extrapair paternity and is available for a large number of species. In contrast to recent studies, we found strong and consistent effects of social mating system on most forms of dimorphism. Social mating system strongly influenced dimorphism in plumage, body mass, and wing length and had some effect on dimorphism in tail length. Sexual dimorphism was relatively greater in species with polygynous or lekking than monogamous mating systems. This was true when we used both species and phylogenetically independent contrasts for analysis. Relative testis size was also related positively to dimorphism in tail and wing length, but in most analyses it was a poorer predictor of plumage dimorphism than social mating system. There was no association between relative testis size and mass dimorphism. Geographic region and life history were also associated with the four types of dimorphism, although their influence varied between the different types of dimorphism. Although there is much interest in the effects of sperm competition on sexual dimorphism, we suggest that traditional explanations based on social mating systems are better predictors of dimorphism in birds.     

Mating unplugged: a model for the evolution of mating plug (dis-)placement

Mating plugs are male-derived structures that may impede female remating by physically obstructing the female genital tract. Although mating plugs exist in many taxa, the forces shaping their evolution are poorly understood. A male can clearly benefit if his mating plug secures his paternity. It is unclear, however, how plug efficacy can be maintained over evolutionary time in the face of counteracting selection on males' ability to remove any plugs placed by their rivals. Here, I present a game-theory model and a simulation model to address this problem. The models predict that evolutionarily stable levels of mating-plug efficacy should be high when (1) the number of mating attempts per female is low; (2) the sex ratio is male-biased, and (3) males are sperm-limited. I discuss these results in the light of empirical data.     

The evolution of plant reproductive systems: how often are transitions irreversible?

Flowering plants are characterized by striking variation in reproductive systems, and the evolutionary lability of their sexual traits is often considered a major driver of lineage diversification. But, evolutionary transitions in reproductive form and function are never entirely unconstrained and many changes exhibit strong directionality. Here, I consider why this occurs by examining transitions in pollination, mating and sexual systems, some of which have been considered irreversible. Among pollination systems, shifts from bee to hummingbird pollination are rarely reversible, whereas transitions from animal to wind pollination are occasionally reversed. Specialized pollination systems can become destabilized through a loss of pollinator service resulting in a return to generalized pollination, or more commonly a reliance on self-pollination. Homomorphic and heteromorphic self-incompatibility systems have multiple origins but breakdown to self-compatibility occurs much more frequently with little evidence for subsequent gains, at least over short time-spans. Similarly, numerous examples of the shift from outcrossing to predominant self-fertilization are known, but cases of reversal are very limited supporting the view that autogamy usually represents an evolutionary dead-end. The evolution of dioecy from hermaphroditism has also been considered irreversible, although recent evidence indicates that the occurrence of sex inconstancy and hybridization can lead to the origin of derived sexual systems from dioecy. The directionality of many transitions clearly refutes the notion of unconstrained reproductive flexibility, but novel adaptive solutions generally do not retrace earlier patterns of trait evolution.     

Experimental evolution under varying sex ratio and nutrient availability modulates male mating success in Drosophila melanogaster

Biased population sex ratios can alter optimal male mating strategies, and allocation to reproductive traits depends on nutrient availability. However, there is little information on how nutrition interacts with sex ratio to influence the evolution of pre-copulatory and post-copulatory traits separately. To address this omission, we test how male mating success and reproductive investment evolve under varying sex ratios and adult diet in Drosophila melanogaster, using experimental evolution. We found that sex ratio and nutrient availability interacted to determine male pre-copulatory performance. Males from female-biased populations were slow to mate when they evolved under protein restriction. By contrast, we found direct and non-interacting effects of sex ratio and nutrient availability on post-copulatory success. Males that evolved under protein restriction were relatively poor at suppressing female remating. Males that evolved under equal sex ratios fathered more offspring and were better at supressing female remating, relative to males from male-biased or female-biased populations. These results support the idea that sex ratios and nutrition interact to determine the evolution of pre-copulatory mating traits, but independently influence the evolution of post-copulatory traits.     

A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora

To critically examine the relationship between species recognized by phylogenetic and reproductive compatibility criteria, we applied phylogenetic species recognition (PSR) to the fungus in which biological species recognition (BSR) has been most comprehensively applied, the well-studied genus Neurospora. Four independent anonymous nuclear loci were characterized and sequenced from 147 individuals that were representative of all described outbreeding species of Neurospora. We developed a consensus-tree approach that identified monophyletic genealogical groups that were concordantly supported by the majority of the loci, or were well supported by at least one locus but not contradicted by any other locus. We recognized a total of eight phylogenetic species, five of which corresponded with the five traditional biological species, and three of which were newly discovered. Not only were phylogenetic criteria superior to traditional reproductive compatibility criteria in revealing the full species diversity of Neurospora, but also significant phylogenetic subdivisions were detected within some species. Despite previous suggestions of hybridization between N. crassa and N. intermedia in nature, and the fact that several putative hybrid individuals were included in this study, no molecular evidence in support of recent interspecific gene flow or the existence of true hybrids was observed. The sequence data from the four loci were combined and used to clarify how the species discovered by PSR were related. Although species-level clades were strongly supported, the phylogenetic relationships among species remained difficult to resolve, perhaps due to conflicting signals resulting from differential lineage sorting.     

The evolution of between‐species reproductive interference capability under different within‐species mating regimes

Sexual selection sometimes favors male traits that benefit their bearers, but harm their mates. The harmful effects of male traits may also extend to females of other species via heterospecific mating interactions. This could affect the coexistence of closely related species during secondary contact. We examined the evolution of the interspecific interfering capability of a beetle (Callosobruchus chinensis) with a congener (C. maculatus) using C. chinensis males reared under conditions of monogamy and polygamy for 17 generations. After experimental evolution, C. chinensis males reared under polygamous conditions imposed greater impacts on offspring production by C. maculatus females than did C. chinensis males reared under monogamous conditions. However, the mechanism by which differential mating regimes altered the effect of C. chinensis males on C. maculatus females was unclear, because we did not find evidence for the expected genital evolution in C. chinensis, despite their body size divergence. Our findings suggest that traits that originally evolved through sexual selection in two allopatric species could influence the coexistence of these species or the likelihood of reinforcement during secondary contact.     

Sexual selection and the evolution of male and female cognition: A test using experimental evolution in seed beetles*

The mating system is thought to be important in shaping animal intelligence and sexual selection has been depicted as a driver of cognitive evolution, either directly by promoting superior cognitive ability during mate competition, or indirectly via genic capture of sexually selected traits. However, it remains unclear if intensified sexual selection leads to general improvements in cognitive abilities. Here, we evaluated this hypothesis by applying experimental evolution in seed beetles. Replicate lines, maintained for 35 generations of either enforced monogamy (eliminating sexual selection) or polygamy, were challenged to locate and discriminate among mates (male assays) or host seeds (female assays) in a spatial chemosensory learning task. All lines displayed learning between trials. Moreover, polygamous males outperformed monogamous males, providing evidence that sexual selection can lead to the evolution of improved male cognition. However, there were no differences between regimes in rates of male learning, and polygamous females showed no improvement in host search and even signs of reduced learning. Hence, sexual selection increased performance in cognitively demanding mate search, but it did not lead to general increases in cognitive abilities. We discuss the possibility that sexually antagonistic selection is an important factor maintaining abundant genetic variation in cognitive traits.     

Adaptation,chance, and history in experimental evolution reversals to unicellularity

Evolution is often deemed irreversible. The evolution of complex traits that require many mutations makes their reversal unlikely. Even in simpler traits, reversals might become less likely as neutral or beneficial mutations, with deleterious effects in the ancestral context, become fixed in the novel background. This is especially true in changes that involve large reorganizations of the organism and its interactions with the environment. The evolution of multicellularity involves the reorganization of previously autonomous cells into a more complex organism; despite the complexity of this change, single cells have repeatedly evolved from multicellular ancestors. These repeated reversals to unicellularity undermine the generality of Dollo's law. In this article, we evaluated the dynamics of reversals to unicellularity from recently evolved multicellular phenotypes of the brewers yeast Saccharomyces cerevisae. Even though multicellularity in this system evolved recently, it involves the evolution of new levels of selection. Strong selective pressures against multicellularity lead to rapid reversibility to single cells in all of our replicate lines, whereas counterselection favoring multicellularity led to minimal reductions to the rates of reversal. History and chance played an important role in the tempo and mode of reversibility, highlighting the interplay of deterministic and stochastic events in evolutionary reversals.     

Rapid courtship evolution in grouse (Tetraonidae): contrasting patterns of acceleration between the Eurasian and North American polygynous clades

Sexual selection is thought to be a powerful diversifying force, based on large ornamental differences between sexually dimorphic species. This assumes that unornamented phenotypes represent evolution without sexual selection. If sexual selection is more powerful than other forms of selection, then two effects would be: rapid divergence of sexually selected traits and a correlation between these divergence rates and variance in mating success in the ornamented sex. I tested for these effects in grouse (Tetraonidae). For three species pairs, within and among polygynous clades, male courtship characters had significantly greater divergence than other characters. This was most pronounced for two species in Tympanuchus. In the Eurasian polygynous clade, relative courtship divergence gradually increased with nucleotide divergence, suggesting a less dramatic acceleration. Increase in relative courtship divergence was associated with mating systems having higher variance in male mating success. These results suggest that sexual selection has accelerated courtship evolution among grouse, although the microevolutionary details appear to vary among clades.     

Sexual selection drives the evolution of antiaphrodisiac pheromones in butterflies

Competition for mates has resulted in sophisticated mechanisms of male control over female reproduction. Antiaphrodisiacs are pheromones transferred from males to females during mating that reduce attractiveness of females to subsequent courting males. Antiaphrodisiacs generally help unreceptive females reduce male harassment. However, lack of control over pheromone release by females and male control over the amount transferred provides males an opportunity to use antiaphrodisiacs to delay remating by females that have returned to a receptive state. We propose a model for the evolution of antiaphrodisiacs under the influence of intrasexual selection, and determine whether changes in this signal in 11 species of Heliconius butterflies are consistent with two predictions of the model. First, we find that as predicted, male-contributed chemical mixtures are complex and highly variable across species, with limited phylogenetic signal. Second, differences in rates of evolution in pheromone composition between two major clades of Heliconius are as expected: the clade with a greater potential for male-male competition (polyandrous) shows a faster rate of divergence than the one with typically monoandrous mating system. Taken together, our results provide evidence that for females, antiaphrodisiacs can be both honest signals of receptivity (helping reduce harassment) and chastity belts (a male-imposed reduction in remating).     

Sexual selection uncouples the evolution of brain and body size in pinnipeds

The size of the vertebrate brain is shaped by a variety of selective forces. Although larger brains (correcting for body size) are thought to confer fitness advantages, energetic limitations of this costly organ may lead to trade-offs, for example as recently suggested between sexual traits and neural tissue. Here, we examine the patterns of selection on male and female brain size in pinnipeds, a group where the strength of sexual selection differs markedly among species and between the sexes. Relative brain size was negatively associated with the intensity of sexual selection in males but not females. However, analyses of the rates of body and brain size evolution showed that this apparent trade-off between sexual selection and brain mass is driven by selection for increasing body mass rather than by an actual reduction in male brain size. Our results suggest that sexual selection has important effects on the allometric relationships of neural development.     

Sexual cannibalism in the fishing spider and a model for the evolution of sexual cannibalism based on genetic constraints

Several hypotheses have been proposed for the evolution of sexual cannibalism by females. Newman and Elgar (1991) suggested that sexual cannibalism prior to mating by virgin female spiders may have evolved as a result of female foraging considerations. According to this model, an adult female's decision to mate or cannibalize a courting male should be based on an assessment of the male's value as a meal versus his value as a mate. The current study provides an empirical test of the assumptions and predictions of this model in the sexually cannibalistic fishing spider. Adult females were subjected to different food treatments, and exposed to adult males in the laboratory. However, only one of the assumptions of the model and none of its five predictions were upheld. We failed to find any effects of female foraging, female mating status, female size, male size or time of the season on females' behaviour towards courting males. Females behaved stereotypically, and many females were left unmated despite numerous mating opportunities. We also demonstrate costs of sexual cannibalism in a natural population. We propose that the act of sexual cannibalism in the fishing spider is non-adaptive, and develop a model for the evolution of premating sexual cannibalism in spiders based on genetic constraints. According to this hypothesis, sexual cannibalism by adult females may have evolved as an indirect result of selection for high and non-discriminate aggression during previous ontogenetic stages. Genetic covariance between different components of aggressive behaviour may constrain the degree to which (1) juvenile and adult aggression and/or (2) aggression towards conspecifics and heterospecifics can vary independently. We briefly review the support for our model, and suggest several critical tests that may be used to assess the assumptions and predictions of the model.