The joint evolution of mating system and pollen performance: Predictions regarding male gametophytic evolution in selfers vs. outcrossers

Studies of sexual selection in plants historically have focused on pollinator attraction, pollen transfer, gametophytic competition, and post-fertilization discrimination by maternal plants. Pollen performance (the speeds of germination and pollen tube growth) in particular is thought to be strongly subject to intrasexual selection, but the effect of mating system on this process has not been rigorously evaluated. Here we propose four predictions derived from the logic that pollen performance should evolve with mating system as an adaptive response to: (1) the competitive environment among pollen genotypes and (2) variation among female genotypes regularly encountered by a given pollen genotype. First, as previously predicted, due to the higher potential for intense selection among diverse pollen genotypes in outcrossing relative to selfing taxa, pollen should evolve to germinate and/or to grow more rapidly in outcrossers than in selfers. Second, due to stronger selection on pollen performance in outcrossing than in selfing taxa, heritable variation in pollen tube growth rate is more likely to be purged in outcrossers. In selfers, by contrast, genetic variation in pollen tube growth rates may readily accumulate because selfing reduces the number of genetically distinct male gametophytes likely to be deposited on any given stigma, thereby relaxing selection on male gametophytic traits. A summary of published studies presented here provides preliminary support for this prediction. Third, due to the high probability that the pollen of outcrossing individuals will be exposed to multiple pistil genotypes, we predict that the pollen of habitually outcrossing taxa will evolve to perform more consistently across female genotypes than the pollen of selfing taxa. Fourth, we predict that epistatic interactions between pollen and pistil genotypes are more likely to evolve in selfers than in outcrossers. We suggest several empirical approaches that may be used to test these predictions.     

Offspring social network structure predicts fitness in families

Social structures such as families emerge as outcomes of behavioural interactions among individuals, and can evolve over time if families with particular types of social structures tend to leave more individuals in subsequent generations. The social behaviour of interacting individuals is typically analysed as a series of multiple dyadic (pair-wise) interactions, rather than a network of interactions among multiple individuals. However, in species where parents feed dependant young, interactions within families nearly always involve more than two individuals simultaneously. Such social networks of interactions at least partly reflect conflicts of interest over the provision of costly parental investment. Consequently, variation in family network structure reflects variation in how conflicts of interest are resolved among family members. Despite its importance in understanding the evolution of emergent properties of social organization such as family life and cooperation, nothing is currently known about how selection acts on the structure of social networks. Here, we show that the social network structure of broods of begging nestling great tits Parus major predicts fitness in families. Although selection at the level of the individual favours large nestlings, selection at the level of the kin-group primarily favours families that resolve conflicts most effectively.     

Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection

It is now widely accepted that post-zygotic reproductive isolation is the result of negative epistatic interactions between derived alleles fixed independently at different loci in diverging populations (the Dobzhansky-Muller model). What is less clear is the nature of the loci involved and whether the derived alleles increase in frequency through genetic drift, or as a result of natural or sexual selection. If incompatible alleles are fixed by selection, transient polymorphisms will be rare and clines for these alleles will be steep where divergent populations meet. If they evolve by drift, populations are expected to harbour substantial genetic variation in compatibility and alleles will introgress across hybrid zones once they recombine onto a genetic background with which they are compatible. Here we show that variation in male sterility in a naturally occurring Chorthippus parallelus grasshopper hybrid zone conforms to the neutral expectations. Asymmetrical clines for male sterility have long tails of introgression and populations distant from the zone centre show significant genetic variation for compatibility. Our data contrast with recent observations on 'speciation genes' that have diverged as a result of strong natural selection.     

Evolution of evolvability in a developmental model

Evolvability, the ability of populations to adapt, can evolve through changes in the mechanisms determining genetic variation and in the processes of development. Here we construct and evolve a simple developmental model in which the pleiotropic effects of genes can evolve. We demonstrate that selection in a changing environment favors a specific pattern of variability, and that this favored pattern maximizes evolvability. Our analysis shows that mutant genotypes with higher evolvability are more likely to increase to fixation. We also show that populations of highly evolvable genotypes are much less likely to be invaded by mutants with lower evolvability, and that this dynamic primarily shapes evolvability. We examine several theoretical objections to the evolution of evolvability in light of this result. We also show that this result is robust to the presence or absence of recombination, and explore how nonrandom environmental change can select for a modular pattern of variability.     

Laboratory evolution of adenylyl cyclase independent learning in Drosophila and missing heritability

Gene interactions are acknowledged to be a likely source of missing heritability in large‐scale genetic studies of complex neurological phenotypes. However, involvement of rare variants, de novo mutations, genetic lesions that are not easily detected with commonly used methods and epigenetic factors also are possible explanations. We used a laboratory evolution study to investigate the modulatory effects of background genetic variation on the phenotypic effect size of a null mutation with known impact on olfactory learning. To accomplish this, we first established a population that contained variation at just 23 loci and used selection to evolve suppression of the learning defect seen with null mutations in the rutabaga adenylyl cyclase. We thus biased the system to favor relatively simplified outcomes by choosing a Mendelian trait and by restricting the genetic variation segregating in the population. This experimental design also assures that the causal effects are among the known 23 segregating loci. We observe a robust response to selection that requires the presence of the 23 variants. Analyses of the underlying genotypes showed that interactions between more than two loci are likely to be involved in explaining the selection response, with implications for the missing heritability problem.     

The evolution of stability in a competitive system

The characteristics governing the dynamics of populations can evolve and this evolution can either be towards stability or chaos. Yet it is not obvious how or why such population characteristics can evolve through selection on individuals. In this paper we construct a mathematical model, inspired by experimental results, illustrating the dynamics of a population of competing Drosophila. We demonstrate how selection of life history characteristics and stability influence one another as a population interacts with its environment. We generalize this result and show that population stability can evolve as a consequence of selection on individuals.     

Evolution of Specificity in Protein-Protein Interactions

Hub proteins are proteins that maintain promiscuous molecular recognition. Because they are reported to play essential roles in cellular control, there has been a special interest in the study of their structural and functional properties, yet the mechanisms by which they evolve to maintain functional interactions are poorly understood. By combining biophysical simulations of coarse-grained proteins and analysis of proteins-complex crystallographic structures, we seek to elucidate those mechanisms. We focus on two types of hub proteins: Multi hubs, which interact with their partners through different interfaces, and Singlish hubs, which do so through a single interface. We show that loss of structural stability is required for the evolution of protein-protein-interaction (PPI) networks, and it is more profound in Singlish hub systems. In addition, different ratios of hydrophobic to electrostatic interfacial amino acids are shown to support distinct network topologies (i.e., Singlish and Multi systems), and therefore underlie a fundamental design principle of PPI in a crowded environment. We argue that the physical nature of hydrophobic and electrostatic interactions, in particular, their favoring of either same-type interactions (hydrophobic-hydrophobic), or opposite-type interactions (negatively-positively charged) plays a key role in maintaining the network topology while allowing the protein amino acid sequence to evolve.     

Evolution of Specificity in Protein-Protein Interactions

Hub proteins are proteins that maintain promiscuous molecular recognition. Because they are reported to play essential roles in cellular control, there has been a special interest in the study of their structural and functional properties, yet the mechanisms by which they evolve to maintain functional interactions are poorly understood. By combining biophysical simulations of coarse-grained proteins and analysis of proteins-complex crystallographic structures, we seek to elucidate those mechanisms. We focus on two types of hub proteins: Multi hubs, which interact with their partners through different interfaces, and Singlish hubs, which do so through a single interface. We show that loss of structural stability is required for the evolution of protein-protein-interaction (PPI) networks, and it is more profound in Singlish hub systems. In addition, different ratios of hydrophobic to electrostatic interfacial amino acids are shown to support distinct network topologies (i.e., Singlish and Multi systems), and therefore underlie a fundamental design principle of PPI in a crowded environment. We argue that the physical nature of hydrophobic and electrostatic interactions, in particular, their favoring of either same-type interactions (hydrophobic-hydrophobic), or opposite-type interactions (negatively-positively charged) plays a key role in maintaining the network topology while allowing the protein amino acid sequence to evolve.     

Stability and the evolvability of function in a model protein

Functional proteins must fold with some minimal stability to a structure that can perform a biochemical task. Here we use a simple model to investigate the relationship between the stability requirement and the capacity of a protein to evolve the function of binding to a ligand. Although our model contains no built-in tradeoff between stability and function, proteins evolved function more efficiently when the stability requirement was relaxed. Proteins with both high stability and high function evolved more efficiently when the stability requirement was gradually increased than when there was constant selection for high stability. These results show that in our model, the evolution of function is enhanced by allowing proteins to explore sequences corresponding to marginally stable structures, and that it is easier to improve stability while maintaining high function than to improve function while maintaining high stability. Our model also demonstrates that even in the absence of a fundamental biophysical tradeoff between stability and function, the speed with which function can evolve is limited by the stability requirement imposed on the protein.     

Nongenetic inheritance and the evolution of costly female preference

In species where males provide neither direct benefits nor paternal care, it is typically assumed that female preferences are maintained by indirect selection reflecting genetic benefits to offspring of preferred males. However, it remains unclear whether populations harbour sufficient genetic variation in fitness to support costly female preferences – a problem called the ‘lek paradox’. Here, we ask whether indirect selection on female preferences can be maintained by nongenetic inheritance. We construct a general model that can be used to represent either genetic or nongenetic inheritance, depending on the choice of parameter values. Interestingly, we find that costly preference is most likely to evolve and persist when fitness depends on an environmentally induced factor that can be transmitted over a single generation only, such as an environment‐dependent paternal effect. Costly preference can also be supported when fitness depends on a highly mutable factor that can persist over multiple generations, such as an epigenetic mark, but the necessary conditions are more restrictive. Our findings show that nongenetic inheritance provides a plausible hypothesis for the maintenance of costly female preferences in species where males provide no direct benefits to females. Nongenetic paternal inheritance of fitness can occur in species lacking conventional forms of paternal care. Indeed, transmission of paternal condition via sperm‐borne nongenetic factors may be more likely to evolve than conventional forms of paternal investment because sperm‐borne effects are protected from cuckoldry. Our results furnish a novel example of an interaction between genetic and nongenetic inheritance that can lead to otherwise unexpected evolutionary outcomes.     

Sequence-structure signals of 3D domain swapping in proteins

Three-dimensional domain swapping occurs when two or more identical proteins exchange identical parts of their structure to generate an oligomeric unit. It affects proteins with diverse sequences and structures, and is expected to play important roles in evolution, functional regulation and even conformational diseases. Here, we search for traces of domain swapping in the protein sequence, by means of algorithms that predict the structure and stability of proteins using database-derived potentials. Regions whose sequences are not optimal with regard to the stability of the native structure, or showing marked intrinsic preferences for non-native conformations in absence of tertiary interactions are detected in most domain-swapping proteins. These regions are often located in areas crucial in the swapping process and are likely to influence it on a kinetic or thermodynamic level. In addition, cation-pi interactions are frequently observed to zip up the edges of the interface between intertwined chains or to involve hinge loop residues, thereby modulating stability. We end by proposing a set of mutations altering the swapping propensities, whose experimental characterization would contribute to refine our in silico derived hypotheses.     

Social structure modulates the evolutionary consequences of social plasticity: A social network perspective on interacting phenotypes

Organisms express phenotypic plasticity during social interactions. Interacting phenotype theory has explored the consequences of social plasticity for evolution, but it is unclear how this theory applies to complex social structures. We adapt interacting phenotype models to general social structures to explore how the number of social connections between individuals and preference for phenotypically similar social partners affect phenotypic variation and evolution. We derive an analytical model that ignores phenotypic feedback and use simulations to test the predictions of this model. We find that adapting previous models to more general social structures does not alter their general conclusions but generates insights into the effect of social plasticity and social structure on the maintenance of phenotypic variation and evolution. Contribution of indirect genetic effects to phenotypic variance is highest when interactions occur at intermediate densities and decrease at higher densities, when individuals approach interacting with all group members, homogenizing the social environment across individuals. However, evolutionary response to selection tends to increase at greater network densities as the effects of an individual's genes are amplified through increasing effects on other group members. Preferential associations among similar individuals (homophily) increase both phenotypic variance within groups and evolutionary response to selection. Our results represent a first step in relating social network structure to the expression of social plasticity and evolutionary responses to selection.     

Population structure and evolutionary progress

Wright's shifting-balance theory is discussed as an example of a process that can cause species to evolve combinations of characters that could not evolve under natural selection alone. A review of the existing theory of peak shifts indicates that the conditions of extreme isolation that are necessary to permit genetic drift to alter the outcome of natural selection in local populations would make gene flow too weak to spread a new combination of genes to other populations in a reasonable time. Instead, it seems likely that major demographic changes must occur in a species for the shifting-balance process to work. A discussion of direct and indirect studies of gene flow in natural populations suggests that the current genetic structure of many species is likely to reflect past demographic events rather than ongoing gene flow. It is possible then that demographic processes could be responsible for spreading new traits in a species, but that would be true whether those new traits evolved only owing to natural selection or owing in addition to genetic drift and other forces.     

The consequences of direct versus indirect species interactions to selection on traits: pollination and nectar robbing in Ipomopsis aggregata

Organisms experience a complex suite of species interactions. Although the ecological consequences of direct versus indirect species interactions have received attention, their evolutionary implications are not well understood. I examined selection on floral traits through direct versus indirect pathways of species interactions using the plant Ipomopsis aggregata and its pollinators and nectar robber. Using path analysis and structural equation modeling, I tested competing hypotheses comparing the relative importance of direct (pollinator-mediated) versus indirect (robber-mediated) interactions to trait selection through female plant function in 2 years. The hypothesis that provided the best fit to the observed data included robbing and pollination, suggesting that both interactors are important in driving selection on some traits; however, the direction and intensity of selection through robbing versus pollination varied between years. I then increased my scope of inference by assessing traits and species interactions across more years. I found that the potential for temporal variation in the direction and intensity of selection was pronounced. Taken together, results suggest that assessing the broader context in which organisms evolve, including both direct and indirect interactions and across multiple years, can provide increased mechanistic understanding of the diversity of ways that animals shape floral and plant evolution.     

Chaotic gene regulatory networks can be robust against mutations and noise

Robustness to mutations and noise has been shown to evolve through stabilizing selection for optimal phenotypes in model gene regulatory networks. The ability to evolve robust mutants is known to depend on the network architecture. How do the dynamical properties and state-space structures of networks with high and low robustness differ? Does selection operate on the global dynamical behavior of the networks? What kind of state-space structures are favored by selection? We provide damage propagation analysis and an extensive statistical analysis of state spaces of these model networks to show that the change in their dynamical properties due to stabilizing selection for optimal phenotypes is minor. Most notably, the networks that are most robust to both mutations and noise are highly chaotic. Certain properties of chaotic networks, such as being able to produce large attractor basins, can be useful for maintaining a stable gene-expression pattern. Our findings indicate that conventional measures of stability, such as damage propagation, do not provide much information about robustness to mutations or noise in model gene regulatory networks.     

Countergradient variation in behaviour,growth and lipid storage in Atlantic cod; environmental and genetic effects

We housed offspring from northern (70° N) and southern (60° N) coastal cod (Gadus morhua) together in a ‘common garden’ rearing experiment at a temperature and light regime representative of the southern population. Through a more active feeding behaviour and a higher success, the northern cod achieved a larger food share and a higher growth rate and condition than their southern conspecifics. This is contrary to what was demonstrated by field data of fish from their natural habitats. The northern cod also allocated more energy to the liver throughout the experiment. Our results agree with the theory of countergradient variation, suggesting that genetic influences on growth and condition have been opposed by environmental constraints in their natural habitat. The observation that the offspring from these populations differ in behavior and growth when housed together support the idea that the growth response to selection would be through a behavioral response. The field data suggest that density‐dependent population process and high juvenile density relative to prey limit the growth and condition in the wild and not necessarily the length of the growth season per se as assumed in the literature. The topographic distance (over 2000 km) limit mixing of early life stages of cod from the northern and southern population, and the different environmental stimuli (seasonality, temperature, food‐web interactions and habitat heterogeneity) in north and south are likely to evolve genetic differences.     

Does behaviour explain the larval dispersal of coral reef fishes better than oceanography?– An individual based model simulation approach

We housed offspring from northern (70° N) and southern (60° N) coastal cod ( Gadus morhua ) together in a 'common garden' rearing experiment at a temperature and light regime representative of the southern population. Through a more active feeding behaviour and a higher success, the northern cod achieved a larger food share and a higher growth rate and condition than their southern conspecifics. This is contrary to what was demonstrated by field data of fish from their natural habitats. The northern cod also allocated more energy to the liver throughout the experiment. Our results agree with the theory of countergradient variation, suggesting that genetic influences on growth and condition have been opposed by environmental constraints in their natural habitat. The observation that the offspring from these populations differ in behavior and growth when housed together support the idea that the growth response to selection would be through a behavioral response.
The field data suggest that density‐dependent population process and high juvenile density relative to prey limit the growth and condition in the wild and not necessarily the length of the growth season per se as assumed in the literature. The topographic distance (over 2000 km) limit mixing of early life stages of cod from the northern and southern population, and the different environmental stimuli (seasonality, temperature, food‐web interactions and habitat heterogeneity) in north and south are likely to evolve genetic differences.     

The tempo and mode of three-dimensional morphological evolution in male reproductive structures

Various evolutionary forces may shape the evolution of traits that influence the mating decisions of males and females. Phenotypic traits that males and females use to judge the species identify of potential mates should evolve in a punctuated fashion, changing significantly at the time of speciation but changing little between speciation events. In contrast, traits experiencing sexual selection or sexually antagonistic interactions are generally expected to change continuously over time because of the directional selection pressures imposed on one sex by the actions of the other. To test these hypotheses, we used spherical harmonic representations of the shapes of male mating structures in reconstructions of the evolutionary tempo of these structures across the history of the Enallagma damselfly clade. Our analyses show that the evolution of these structures is completely consistent with a punctuated model of evolutionary change and a constant evolutionary rate throughout the clade's history. In addition, no interpopulation variation in shape was detected across the range of one species. These results indicate that male mating structures in this genus are used primarily for identifying the species of potential mates and experience little or no selection from intraspecific sexual selection or sexual antagonism. The implications of these results for speciation are discussed.     

Structural diversity of domain superfamilies in the CATH database

The CATH database of domain structures has been used to explore the structural variation of homologous domains in 294 well populated domain structure superfamilies, each containing at least three sequence diverse relatives. Our analyses confirm some previously detected trends relating sequence divergence to structural variation but for a much larger dataset and in some superfamilies the new data reveal exceptional structural variation. Use of a new algorithm (2DSEC) to analyse variability in secondary structure compositions across a superfamily sheds new light on how structures evolve. 2DSEC detects inserted secondary structures that embellish the core of conserved secondary structures found throughout the superfamily. Analysis showed that for 56% of highly populated superfamilies (>9 sequence diverse relatives), there are twofold or more increases in the numbers of secondary structures in some relatives. In some families fivefold increases occur, sometimes modifying the fold of the domain. Manual inspection of secondary structure insertions or embellishments in 48 particularly variable superfamilies revealed that although these insertions were usually discontiguous in the sequence they were often co-located in 3D resulting in a larger structural motif that often modified the geometry of the active site or the surface conformation promoting diverse domain partnerships and protein interactions. These observations, supported by automatic analysis of all well populated CATH families, suggest that accretion of small secondary structure insertions may provide a simple mechanism for evolving new functions in diverse relatives. Some layered domain architectures (e.g. mainly-beta and alpha-beta sandwiches) that recur highly in the genomes more frequently exploit these types of embellishments to modify function. In these architectures, aggregation occurs most often at the edges, top or bottom of the beta-sheets. Information on structural variability across domain superfamilies has been made available through the CATH Dictionary of Homologous Structures (DHS).     

Male–female genotype interactions maintain variation in traits important for sexual interactions and reproductive isolation

Prezygotic reproductive isolation can evolve quickly when sexual selection drives divergence in traits important for sexual interactions between populations. It has been hypothesized that standing variation for male/female traits and preferences facilitates this rapid evolution and that variation in these traits is maintained by male–female genotype interactions in which specific female genotypes prefer specific male traits. This hypothesis can also explain patterns of speciation when ecological divergence is lacking, but this remains untested because it requires information about sexual interactions in ancestral lineages. Using a set of ancestral genotypes that previously had been identified as evolving reproductive isolation, we specifically asked whether there is segregating variation in female preference and whether segregating variation in sexual interactions is a product of male–female genotype interactions. Our results provide evidence for segregating variation in female preference and further that male–female genotype interactions are important for maintaining variation that selection can act on and that can lead to reproductive isolation.