The draft genome of a socially polymorphic halictid bee,Lasioglossum albipes

Background

Taxa that harbor natural phenotypic variation are ideal for ecological genomic approaches aimed at understanding how the interplay between genetic and environmental factors can lead to the evolution of complex traits. Lasioglossum albipes is a polymorphic halictid bee that expresses variation in social behavior among populations, and common-garden experiments have suggested that this variation is likely to have a genetic component.

Results

We present the L. albipes genome assembly to characterize the genetic and ecological factors associated with the evolution of social behavior. The de novo assembly is comparable to other published social insect genomes, with an N50 scaffold length of 602 kb. Gene families unique to L. albipes are associated with integrin-mediated signaling and DNA-binding domains, and several appear to be expanded in this species, including the glutathione-s-transferases and the inositol monophosphatases. L. albipes has an intact DNA methylation system, and in silico analyses suggest that methylation occurs primarily in exons. Comparisons to other insect genomes indicate that genes associated with metabolism and nucleotide binding undergo accelerated evolution in the halictid lineage. Whole-genome resequencing data from one solitary and one social L. albipes female identify six genes that appear to be rapidly diverging between social forms, including a putative odorant receptor and a cuticular protein.

Conclusions

L. albipes represents a novel genetic model system for understanding the evolution of social behavior. It represents the first published genome sequence of a primitively social insect, thereby facilitating comparative genomic studies across the Hymenoptera as a whole.     

Same-Sex Twin Pair Phenotypic Correlations are Consistent with Human <Emphasis Type="Italic">Y</Emphasis> Chromosome Promoting Phenotypic Heterogeneity

Junk DNA has been long appreciated as an evolutionary facilitator because it can participate in the causation of genetic variation such as chromosome rearrangements and can be exapted into coding or regulatory elements. Recently, it has been proposed that junk DNA variation within natural populations indirectly causes a phenotypic heterogeneity that subsequently promotes genetic capacitance, i.e., the random fluctuation of genetic variation. Junk DNA role as capacitor might drive population traits such as sexual dimorphism, spatiotemporal dynamics, or genetic diversification leading into speciation. Whether the human species also showed junk DNA-based capacitance manifested as a junk DNA-dependent phenotypic heterogeneity that contributed to the etiology and expression of diseases or the evolutionary history of human populations is intriguing. Because the human Y chromosome is highly enriched in junk DNA, humans are sexually dimorphic for the genomic content in junk DNA. Thus, it would be expected that junk DNA-based capacitance in humans were manifested as a sexual dimorphism for phenotypic heterogeneity. Here, I gather supporting evidence for the existence of a sexual dimorphism for putative junk DNA-based phenotypic heterogeneity by analyzing same-sex twin pairs phenotypic concordance.     

INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS: I. DIRECT AND INDIRECT GENETIC EFFECTS OF SOCIAL INTERACTIONS

Interacting phenotypes are traits whose expression is affected by interactions with conspecifics. Commonly-studied interacting phenotypes include aggression, courtship, and communication. More extreme examples of interacting phenotypes—traits that exist exclusively as a product of interactions—include social dominance, intraspecific competitive ability, and mating systems. We adopt a quantitative genetic approach to assess genetic influences on interacting phenotypes. We partition genetic and environmental effects so that traits in conspecifics that influence the expression of interacting phenotypes are a component of the environment. When the trait having the effect is heritable, the environmental influence arising from the interaction has a genetic basis and can be incorporated as an indirect genetic effect. However, because it has a genetic basis, this environmental component can evolve. Therefore, to consider the evolution of interacting phenotypes we simultaneously consider changes in the direct genetic contributions to a trait (as a standard quantitative genetic approach would evaluate) as well as changes in the environmental (indirect genetic) contribution to the phenotype. We then explore the ramifications of this model of inheritance on the evolution of interacting phenotypes. The relative rate of evolution in interacting phenotypes can be quite different from that predicted by a standard quantitative genetic analysis. Phenotypic evolution is greatly enhanced or inhibited depending on the nature of the direct and indirect genetic effects. Further, unlike most models of phenotypic evolution, a lack of variation in direct genetic effects does not preclude evolution if there is genetic variance in the indirect genetic contributions. The available empirical evidence regarding the evolution of behavior expressed in interactions, although limited, supports the predictions of our model.     

Tracing the Evolution of Competence in Haemophilus influenzae

Natural competence is the genetically encoded ability of some bacteria to take up DNA from the environment. Although most of the incoming DNA is degraded, occasionally intact homologous fragments can recombine with the chromosome, displacing one resident strand. This potential to use DNA as a source of both nutrients and genetic novelty has important implications for the ecology and evolution of competent bacteria. However, it is not known how frequently competence changes during evolution, or whether non-competent strains can persist for long periods of time. We have previously studied competence in H. influenzae and found that both the amount of DNA taken up and the amount recombined varies extensively between different strains. In addition, several strains are unable to become competent, suggesting that competence has been lost at least once. To investigate how many times competence has increased or decreased during the divergence of these strains, we inferred the evolutionary relationships of strains using the largest datasets currently available. However, despite the use of three datasets and multiple inference methods, few nodes were resolved with high support, perhaps due to extensive mixing by recombination. Tracing the evolution of competence in those clades that were well supported identified changes in DNA uptake and/or transformation in most strains. The recency of these events suggests that competence has changed frequently during evolution but the poor support of basal relationships precludes the determination of whether non-competent strains can persist for long periods of time. In some strains, changes in transformation have occurred that cannot be due to changes in DNA uptake, suggesting that selection can act on transformation independent of DNA uptake.     

A simple mechanism for complex social behavior

The evolution of cooperation is a paradox because natural selection should favor exploitative individuals that avoid paying their fair share of any costs. Such conflict between the self-interests of cooperating individuals often results in the evolution of complex, opponent-specific, social strategies and counterstrategies. However, the genetic and biological mechanisms underlying complex social strategies, and therefore the evolution of cooperative behavior, are largely unknown. To address this dearth of empirical data, we combine mathematical modeling, molecular genetic, and developmental approaches to test whether variation in the production of and response to social signals is sufficient to generate the complex partner-specific social success seen in the social amoeba Dictyostelium discoideum. Firstly, we find that the simple model of production of and response to social signals can generate the sort of apparent complex changes in social behavior seen in this system, without the need for partner recognition. Secondly, measurements of signal production and response in a mutant with a change in a single gene that leads to a shift in social behavior provide support for this model. Finally, these simple measurements of social signaling can also explain complex patterns of variation in social behavior generated by the natural genetic diversity found in isolates collected from the wild. Our studies therefore demonstrate a novel and elegantly simple underlying mechanistic basis for natural variation in complex social strategies in D. discoideum. More generally, they suggest that simple rules governing interactions between individuals can be sufficient to generate a diverse array of outcomes that appear complex and unpredictable when those rules are unknown.     

Phenotypic and genetic integration of personality and growth under competition in the sheepshead swordtail,Xiphophorus birchmanni

Competition for resources including food, physical space, and potential mates is a fundamental ecological process shaping variation in individual phenotype and fitness. The evolution of competitive ability, in particular social dominance, depends on genetic (co)variation among traits causal (e.g., behavior) or consequent (e.g., growth) to competitive outcomes. If dominance is heritable, it will generate both direct and indirect genetic effects (IGE) on resource‐dependent traits. The latter are expected to impose evolutionary constraint because winners necessarily gain resources at the expense of losers. We varied competition in a population of sheepshead swordtails, Xiphophorus birchmanni, to investigate effects on behavior, size, growth, and survival. We then applied quantitative genetic analyses to determine (i) whether competition leads to phenotypic and/or genetic integration of behavior with life history and (ii) the potential for IGE to constrain life history evolution. Size, growth, and survival were reduced at high competition. Male dominance was repeatable and dominant individuals show higher growth and survival. Additive genetic contributions to phenotypic covariance were significant, with the G matrix largely recapitulating phenotypic relationships. Social dominance has a low but significant heritability and is strongly genetically correlated with size and growth. Assuming causal dependence of growth on dominance, hidden IGE will therefore reduce evolutionary potential.     

Phylogenetic relationships of palaearctic formica species (hymenoptera, formicidae) based on mitochondrial cytochrome B sequences

Ants of genus Formica demonstrate variation in social organization and represent model species for ecological, behavioral, evolutionary studies and testing theoretical implications of the kin selection theory. Subgeneric division of the Formica ants based on morphology has been questioned and remained unclear after an allozyme study on genetic differentiation between 13 species representing all subgenera was conducted. In the present study, the phylogenetic relationships within the genus were examined using mitochondrial DNA sequences of the cytochrome b and a part of the NADH dehydrogenase subunit 6. All 23 Formica species sampled in the Palaearctic clustered according to the subgeneric affiliation except F. uralensis that formed a separate phylogenetic group. Unlike Coptoformica and Formica s. str., the subgenus Serviformica did not form a tight cluster but more likely consisted of a few small clades. The genetic distances between the subgenera were around 10%, implying approximate divergence time of 5 Myr if we used the conventional insect divergence rate of 2% per Myr. Within-subgenus divergence estimates were 6.69% in Serviformica, 3.61% in Coptoformica, 1.18% in Formica s. str., which supported our previous results on relatively rapid speciation in the latter subgenus. The phylogeny inferred from DNA sequences provides a necessary framework against which the evolution of social traits can be compared. We discuss implications of inferred phylogeny for the evolution of social traits.     

The influence of multiple inseminations and multiple foundresses on social evolution

The breeding biology of a population determines the way in which individuals are distributed within and between progeny groups and, thus, affects the genetic variation within and between these groups. The breeding biology of any organism can be characterized by the distribution of the numbers of mates of females, the apportionment of paternity among males, the distribution of the numbers of females reproducing in common nests, and the apportionment of total fecundity within a nest among founding females. In addition, the possibility of genetic correlations among mates or among founding females is an important consideration and will be addressed in a later paper. The influence of the breeding biology on social evolution was evaluated by deriving the necessary conditions for the spread of genes for social behaviors and the rate of spread of these genes for populations with different breeding biologies. The first step in this derivation is to demonstrate that selection for genes determining social behavior can be represented as the covariance between gene frequency and relative fitness. Secondly, it is shown that this covariance can be formally partitioned into within and between group components. Thirdly, each covariance component is shown to be equivalent to the product of a genetic variance and a coefficient of linear regression of relative fitness on gene frequency. Lastly, specific models for the genotype fitnesses and breeding biologies are assumed and the necessary conditions for the increase in the frequency of altruistic alleles are obtained. The theory illustrates that variation in the numbers of mates per female has less of an effect on the evolution of social behaviors than does variation in the numbers of reproductive females per nest. In addition, it points out that the harmonic mean number of mates per female or of females per nest is a more useful summary statistic for characterizing populations with respect to the expected degree of evolved sociality than is the arithmetic mean.     

Integrating Proximate and Ultimate Causation in the Study of Vertebrate Behavior: Methods Considerations

SYNOPSIS. Methods issues are critical for the integration ofproximate and ultimate explanations of animal behavior. Understandingthat evolution of behavior may begin with changes in sensoryand perceptual systems is a first step. For example, advancesin neurobiology can trigger questions about social behavior.Variation in the size of particular brain areas, such as thehippocampus, can be related to variation in socio-spatial systems.Second, procedures, developed in recent years, provide new avenuesto understand behavior. Hormone assay techniques, such as RIAand ELISA, can be performed on some hormones from urine andfeces collected in the wild. Metabolic measurement, such asthe use of doublylabeled water, make it possible to measureenergy costs under field conditions. Advances in DNA technologiesprovide new perspectives, particularly with regard to measuringreproductive success. Third, current theories in behavior canbe tested with regard to physiological mechanisms; all thatis needed is some ingenuity to design and execute appropriatestudies. These include kin recognition, sex ratio variation,and foraging behavior. Fourth, cross—fertilization betweenlaboratory and field approaches produces new insights regardingbehavior. Organizational effects of hormones have now been exploredin field populations of mice and in domestic swine. Testingaspects of foraging behavior in the laboratory is another example.Fifth, simulation models have been used to produce new questionsabout both proximate and ultimate aspects of behavior. Exploringbehavioral phenomena may involve semi—natural settings.The suitability of semi—natural enclosures for the studyof house mouse behavior has been tested with regard to densityand home range size.     

INDIRECT GENETIC EFFECTS INFLUENCE ANTIPREDATOR BEHAVIOR IN GUPPIES: ESTIMATES OF THE COEFFICIENT OF INTERACTION PSI AND THE INHERITANCE OF RECIPROCITY

How and why cooperation evolves, particularly among nonrelatives, remains a major paradox for evolutionary biologists and behavioral ecologists. Although much attention has focused on fitness consequences associated with cooperating, relatively little is known about the second component of evolutionary change, the inheritance of cooperation or reciprocity. The genetics of behaviors that can only be expressed in the context of interactions are particularly difficult to describe because the relevant genes reside in multiple social partners. Indirect genetic effects (IGEs) describe the influence of genes carried in social partners on the phenotype of a focal individual and thus provide a novel approach to quantifying the genetics underlying interactions such as reciprocal cooperation. We used inbred lines of guppies and a novel application of IGE theory to describe the dual genetic control of predator inspection and social behavior, both classic models of reciprocity. We identified effects of focal strain, social group strain, and interactions between focal and group strains on variation in focal behavior. We measured ψ, the coefficient of the interaction, which describes the degree to which an individual's phenotype is influenced by the phenotype of its social partners. The genetic identity of social partners substantially influences inspection behavior, measures of threat assessment, and schooling and does so in positively reinforcing manner. We therefore demonstrate strong IGEs for antipredator behavior that represent the genetic variation necessary for the evolution of reciprocity.     

Social context, stress, and plasticity of aging

Positive social contact is an important factor in healthy aging, but our understanding of how social interactions influence senescence is incomplete. As life expectancy continues to increase because of reduced death rates among elderly, the beneficial role of social relationships is emerging as a cross-cutting theme in research on aging and healthspan. There is a need to improve knowledge on how behavior shapes, and is shaped by, the social environment, as well as needs to identify and study biological mechanisms that can translate differences in the social aspects of behavioral efforts, relationships, and stress reactivity (the general physiological and behavioral response-pattern to harmful, dangerous or unpleasant situations) into variation in aging. Honey bees (Apis mellifera) provide a genetic model in sociobiology, behavioral neuroscience, and gerontology that is uniquely sensitive to social exchange. Different behavioral contact between these social insects can shorten or extend lifespan more than 10-fold, and some aspects of their senescence are reversed by social cues that trigger aged individuals to express youthful repertoires of behavior. Here, I summarize how variation in social interactions contributes to this plasticity of aging and explain how beneficial and detrimental roles of social relationships can be traced from environmental and biological effects on honey bee physiology and behavior, to the expression of recovery-related plasticity, stress reactivity, and survival during old age. This system provides intriguing opportunities for research on aging.     

植物分子群体遗传学研究动态

分子群体遗传学是当代进化生物学研究的支柱学科, 也是遗传育种和关于遗传关联作图和连锁分析的基础理论学科。分子群体遗传学是在经典群体遗传的基础上发展起来的, 它利用大分子主要是DNA序列的变异式样来研究群体的遗传结构及引起群体遗传变化的因素与群体遗传结构的关系, 从而使得遗传学家能够从数量上精确地推知群体的进化演变, 不仅克服了经典的群体遗传学通常只能研究群体遗传结构短期变化的局限性, 而且可检验以往关于长期进化或遗传系统稳定性推论的可靠程度。同时, 对群体中分子序列变异式样的研究也使人们开始重新审视达尔文的以“自然选择”为核心的进化学说。到目前为止, 分子群体遗传学已经取得长足的发展, 阐明了许多重要的科学问题, 如一些重要农作物的DNA多态性式样、连锁不平衡水平及其影响因素、种群的变迁历史、基因进化的遗传学动力等, 更为重要的是, 在分子群体遗传学基础上建立起来的新兴的学科如分子系统地理学等也得到了迅速的发展。文中综述了植物分子群体遗传研究的内容及最新成果。     

Genome‐wide signature of local adaptation linked to variable CpG methylation in oak populations

It has long been known that adaptive evolution can occur through genetic mutations in DNA sequence, but it is unclear whether adaptive evolution can occur through analogous epigenetic mechanisms, such as through DNA methylation. If epigenetic variation contributes directly to evolution, species under threat of disease, invasive competition, climate change or other stresses would have greater stores of variation from which to draw. We looked for evidence of natural selection acting on variably methylated DNA sites using population genomic analysis across three climatologically distinct populations of valley oaks. We found patterns of genetic and epigenetic differentiations that indicate local adaptation is operating on large portions of the oak genome. While CHG methyl polymorphisms are not playing a significant role and would make poor targets for natural selection, our findings suggest that CpG methyl polymorphisms as a whole are involved in local adaptation, either directly or through linkage to regions under selection.     

Genetic Color Morphs in the Eastern Mosquitofish Experience Different Social Environments in the Wild and Laboratory

The social environment of an animal is an especially interesting component of its environment because it can be shaped by both genetic and non‐genetic variation among social partners. Indirect genetic effects (IGEs) are those created when genetic variation in social partners contributes to variation in an individual's phenotype; a potentially common form of IGE occurs when the expression of a behavioral phenotype depends on the particular genotypic combination of interacting individuals. Although IGEs can profoundly affect individual‐ and group‐level fitness, population dynamics, and even community structure, understanding their importance is complicated by two inherent challenges: (1) identifying individuals with genetic differences in social interactions that can contribute to IGEs and (2) characterizing natural social interactions that potentially involve IGEs. As a first step toward addressing both these challenges in the same system, we investigated social interactions involving genetically distinct male color morphs in the poeciliid fish Gambusia holbrooki under natural and laboratory conditions. Previous work indicates that melanic (M) and silver (S) males differ in social behavior and in how conspecifics respond to them, suggesting the potential for IGEs. We used a combination of live and video recording of social groups in two natural populations and in the laboratory to determine the potential for IGEs to contribute to behavioral variation in this species. We found that M males had more social partners, and especially more female social partners than did S males, in nature and in the laboratory. These results suggest that both direct and indirect genetic effects have the potential to play a role in the expression and evolution of social behavior in G. holbrooki.     

Why do species vary in their rate of molecular evolution?

Despite hopes that the processes of molecular evolution would be simple, clock-like and essentially universal, variation in the rate of molecular evolution is manifest at all levels of biological organization. Furthermore, it has become clear that rate variation has a systematic component: rate of molecular evolution can vary consistently with species body size, population dynamics, lifestyle and location. This suggests that the rate of molecular evolution should be considered part of life-history variation between species, which must be taken into account when interpreting DNA sequence differences between lineages. Uncovering the causes and correlates of rate variation may allow the development of new biologically motivated models of molecular evolution that may improve bioinformatic and phylogenetic analyses.     

Choosing the right molecular genetic markers for studying biodiversity: from molecular evolution to practical aspects

The use of molecular genetic markers (MGMs) has become widespread among evolutionary biologists, and the methods of analysis of genetic data improve rapidly, yet an organized framework in which scientists can work is lacking. Elements of molecular evolution are summarized to explain the origin of variation at the DNA level, its measures, and the relationships linking genetic variability to the biological parameters of the studied organisms. MGM are defined by two components: the DNA region(s) screened, and the technique used to reveal its variation. Criteria of choice belong to three categories: (1) the level of variability, (2) the nature of the information (e.g. dominance vs. codominance, ploidy, ... ) which must be determined according to the biological question and (3) some practical criteria which mainly depend on the equipment of the laboratory and experience of the scientist. A three-step procedure is proposed for drawing up MGMs suitable to answer given biological questions, and compiled data are organized to guide the choice at each step: (1) choice, determined by the biological question, of the level of variability and of the criteria of the nature of information, (2) choice of the DNA region and (3) choice of the technique.     

Evolution in heterogeneous environments and the potential of maintenance of genetic variation in traits of adaptive significance

The maintenance of genetic variation in traits of adaptive significance has been a major dilemma of evolutionary biology. Considering the pattern of increased genetic variation associated with environmental clines and heterogeneous environments, selection in heterogeneous environments has been proposed to facilitate the maintenance of genetic variation. Some models examining whether genetic variation can be maintained, in heterogeneous environments are reviewed. Genetic mechanisms that constrain evolution in quantitative genetic traits indicate that genetic variation can be maintained but when is not clear. Furthermore, no comprehensive models have been developed, likely due to the genetic and environmental complexity of this issue. Therefore, I have suggested two empirical approaches to provide insight for future theoretical and empirical research. Traditional path analysis has been a very powerful approach for understanding phenotypic selection. However, it requires substantial information on the biology of the study system to construct a causal model and alternatives. Exploratory path analysis is a data driven approach that uses the statistical relationships in the data to construct a set of models. For example, it can be used for understanding phenotypic selection in different environments, where there is no prior information to develop path models in the different environments. Data from Brassica rapa grown in different nutrients indicated that selection changed in the different environments. Experimental evolutionary studies will provide direct tests as to when genetic variation is maintained.     

Genetic variation and social structure: a case-study from Africa

Understanding the relations between social and biological factors in determining the evolution of human populations is one of the principal aims of bio-anthropological research. The recent introduction of unilinearly transmitted polymorphisms of mitochondrial DNA and Y-chromosome has disclosed new possibilities for the study of bio-cultural evolutionary processes. In this communication, I present a study on the relationships between social structure and genetic variation in sub-Saharan Africa based on published and unpublished mitochondrial and Y-chromosomal data relative to a total of 40 populations. The results obtained reveal a striking difference in the genetic structure of farming (Bantu speakers) and hunting-gathering (Pygmies and Bushmen) populations. To explain this difference, I propose that asymmetric gene flow, polyginy and patrilocality, and hence the socio-cultural factors underlying them, have had an important role in determining and differentiating the genetic structure of sub-Saharan populations. The limits and the implications of this study are discussed.     

In search of polymorphic Alu insertions with restricted geographic distributions

Alu elements are transposable elements that have reached over one million copies in the human genome. Some Alu elements inserted in the genome so recently that they are still polymorphic for insertion presence or absence in human populations. Recently, there has been an increasing interest in using Alu variation for studies of human population genetic structure and inference of individual geographic origin. Currently, this requires a high number of Alu loci. Here, we used a linker-mediated polymerase chain reaction method to preferentially identify low-frequency Alu elements in various human DNA samples with different geographic origins. The candidate Alu loci were subsequently genotyped in 18 worldwide human populations (approximately 370 individuals), resulting in the identification of two new Alu insertions restricted to populations of African ancestry. Our results suggest that it may ultimately become possible to correctly infer the geographic affiliation of unknown samples with high levels of confidence without having to genotype as many as 100 Alu loci. This is desirable if Alu insertion polymorphisms are to be used for human evolution studies or forensic applications.     

Rapid adaptation: a new dimension for evolutionary perspectives in ecology

Although the study of adaptation is central to biology, two types of adaptation are recognized in the biological field: physiological adaptation (accommodation or acclimation; an individual organism’s phenotype is adjusted to its environment) and evolutionary–biological adaptation (adaptation is shaped by natural selection acting on genetic variation). The history of the former concept dates to the late nineteenth and early twentieth centuries, and has more recently been systemized in the twenty-first century. Approaches to the understanding of phenotypic plasticity and learning behavior have only recently been developed, based on cellular–histological and behavioral–neurobiological techniques as well as traditional molecular biology. New developments of the former concepts in phenotypic plasticity are discussed in bacterial persistence, wing di-/polymorphism with transgenerational effects, polyphenism in social insects, and defense traits for predator avoidance, including molecular biology analyses. We also discuss new studies on the concept of genetic accommodation resulting in evolution of phenotypic plasticity through a transgenerational change in the reaction norm based on a threshold model. Learning behavior can also be understood as physiological phenotypic plasticity, associating with the brain–nervous system, and it drives the accelerated evolutionary change in behavioral response (the Baldwin effect) with memory stock. Furthermore, choice behaviors are widely seen in decision-making of animal foragers. Incorporating flexible phenotypic plasticity and learning behavior into modeling can drastically change dynamical behavior of the system. Unification of biological sciences will be facilitated and integrated, such as behavioral ecology and behavioral neurobiology in the area of learning, and evolutionary ecology and molecular developmental biology in the theme of phenotypic plasticity.