More on the genetical theory of multilevel selection

In my article The genetical theory of multilevel selection, I provided a synthesis of the theory of multilevel selection (MLS) and the theory of natural selection in class‐structured populations. I framed this synthesis within Fisher's genetical paradigm, taking a strictly genetical approach to traits and fitness. I showed that this resolves a number of long‐standing conceptual problems that have plagued the MLS literature, including the issues of ‘aggregate’ vs. ‘emergent’ group traits, ‘collective fitness₁’ vs. ‘collective fitness₂’ and ‘MLS1’ vs. ‘MLS2 ‘. In his commentary, Goodnight suggests this theoretical and conceptual synthesis is flawed in several respects. Here, I show this is incorrect, by: reiterating the theoretical and conceptual goals of my synthesis; clarifying that my genetical approach to traits is necessary for a proper analysis of the action of MLS independently of non‐Darwinian factors; emphasizing that the Price–Hamilton approach to MLS provides a consistent, useful and conceptually superior theoretical framework; and explaining the role of reproductive value in the study of natural selection in class‐structured populations. I also show that Goodnight's contextual analysis treatment of MLS in a class‐structured population is mathematically, biologically and conceptually inadequate.     

Low genetic diversity and strong but shallow population differentiation suggests genetic homogenization by metapopulation dynamics in a social spider

Mating systems and population dynamics influence genetic diversity and structure. Species that experience inbreeding and limited gene flow are expected to evolve isolated, divergent genetic lineages. Metapopulation dynamics with frequent extinctions and colonizations may, on the other hand, deplete and homogenize genetic variation, if extinction rate is sufficiently high compared to the effect of drift in local demes. We investigated these theoretical predictions empirically in social spiders that are highly inbred. Social spiders show intranest mating, female‐biased sex ratio, and frequent extinction and colonization events, factors that deplete genetic diversity within nests and populations and limit gene flow. We characterized population genetic structure in Stegodyphus sarasinorum, a social spider distributed across the Indian subcontinent. Species‐wide genetic diversity was estimated over approximately 2800 km from Sri Lanka to Himalayas, by sequencing 16 protein‐coding nuclear loci. We found 13 SNPs in 6592 bp (π = 0.00045) indicating low species‐wide nucleotide diversity. Three genetic lineages were strongly differentiated; however, only one fixed difference among them suggests recent divergence. This is consistent with a scenario of metapopulation dynamics that homogenizes genetic diversity across the species' range. Ultimately, low standing genetic variation may hamper a species' ability to track environmental change and render social inbreeding spiders ‘evolutionary dead‐ends’.     

Within-stand variation in silver birch (Betula pendula Roth) phenology

Key message

Within a local population genotypes differ in the timing of bud burst, but genotypes with early bud burst unfold their leaves slower, resulting in an equal period of carbon gain.

Abstract

The ability of local populations to cope with disturbances like adverse weather events or a changing climate depends on the genotypic richness of such populations, emphasising the importance of differences between genotypes in traits related to growth and survival at this scale. Due to their longevity, these differences are of special importance in trees, yet for trees, differences between genotypes within local populations remain unexplored. The phenological cycle is important in this respect, since a correct timing of phenological events is critical for growth and survival of trees, especially in environments with strong seasonality and changes in the timing of phenological events has consequences for, among others, net ecosystem productivity and the climate system as a whole. In this light accounting for differences in the timing of phenological events within species is currently identified as a research challenge. This study contributes to the knowledge of differences between genotypes on the small spatial scale of a local population. We examined the timing of phenological events of 15 micropropagated silver birch (Betula pendula Roth) genotypes representing a natural population. Measurements covered bud burst (7 years) and leaf unfolding in spring and chlorophyll degradation in autumn (2 years for both). These data were used to estimate the period of carbon gain. Differences between genotypes in the temperature sum required for bud burst were present, with genotypes showing ‘early’ (i.e. a low temperature sum requirement for bud burst) and ‘late’ bud burst across the 7-year study period. Differences were small in most years (i.e. 3 days), but differences of 16 days were recorded within the 7-year study period as well. Genotypes with ‘early’ bud burst were less sensitive to variations in environmental conditions in spring compared to genotypes with ‘late’ bud burst. Differences in bud burst were not carried over to the estimated period of carbon gain. Due to faster leaf expansion in genotypes with ‘late’ bud burst and the lack of differences between genotypes in autumn senescence the estimated period of carbon gain was similar among genotypes.     

Selection for territory acquisition is modulated by social network structure in a wild songbird

The social environment may be a key mediator of selection that operates on animals. In many cases, individuals may experience selection not only as a function of their phenotype, but also as a function of the interaction between their phenotype and the phenotypes of the conspecifics they associate with. For example, when animals settle after dispersal, individuals may benefit from arriving early, but, in many cases, these benefits will be affected by the arrival times of other individuals in their local environment. We integrated a recently described method for calculating assortativity on weighted networks, which is the correlation between an individual's phenotype and that of its associates, into an existing framework for measuring the magnitude of social selection operating on phenotypes. We applied this approach to large‐scale data on social network structure and the timing of arrival into the breeding area over three years. We found that late‐arriving individuals had a reduced probability of breeding. However, the probability of breeding was also influenced by individuals’ social networks. Associating with late‐arriving conspecifics increased the probability of successfully acquiring a breeding territory. Hence, social selection could offset the effects of nonsocial selection. Given parallel theoretical developments of the importance of local network structure on population processes, and increasing data being collected on social networks in free‐living populations, the integration of these concepts could yield significant insights into social evolution.     

Parallel evolution of gene classes,but not genes: Evidence from Hawai'ian honeycreeper populations exposed to avian malaria

Adaptation in nature is ubiquitous, yet characterizing its genomic basis is difficult because population demographics cause correlations with nonadaptive loci. Introduction events provide opportunities to observe adaptation over known spatial and temporal scales, facilitating the identification of genes involved in adaptation. The pathogen causing avian malaria, Plasmodium relictum, was introduced to Hawai'i in the 1930s and elicited extinctions and precipitous population declines in native honeycreepers. After a sharp initial population decline, the Hawai'i ‘amakihi (Chlorodrepanis virens) has evolved tolerance to the parasite at low elevations where P. relictum exists, and can sustain infection without major fitness consequences. High‐elevation, unexposed populations of ‘amakihi display little to no tolerance. To explore the genomic basis of adaptation to P. relictum in low‐elevation ‘amakihi, we genotyped 125 ‘amakihi from the island of Hawai'i via hybridization capture to 40,000 oligonucleotide baits containing SNPs and used the reference ‘amakihi genome to identify genes potentially under selection from malaria. We tested for outlier loci between low‐ and high‐elevation population pairs and identified loci with signatures of selection within low‐elevation populations. In some cases, genes commonly involved in the immune response (e.g., major histocompatibility complex) were associated with malaria presence in the population. We also detected several novel candidate loci that may be implicated in surviving malaria infection (e.g., beta‐defensin, glycoproteins and interleukin‐related genes). Our results suggest that rapid adaptation to pathogens may occur through changes in different immune genes, but in the same classes of genes, across populations.     

Alfred Russel Wallace, past and future

The naturalist Alfred Russel Wallace (1823–1913) has for many years been standing in the shadow of his more famed co‐discoverer of the principle of natural selection, Charles Darwin. Despite outward similarities between the two men's formulation of the principle, Wallace had fit his appreciation of natural selection into views on evolution that were quite different from Darwin's. A closer examination of what Wallace had in mind suggests a model of process in which natural selection per se acts as the negative feedback mechanism (actually, a ‘state‐space’) in the relation between population and environment, and environmental engagement as made possible by the resulting selection of traits acts as the positive feedback part of the cycle. Thus, it may be better to contextualize adaptive structures as entropy‐relaying biogeochemical facilitators that only ‘generate a potential for evolution’ than to portray them as the end results of evolution. This systems point of view better lends itself to appreciations of the biogeographical context of evolution than does the tree‐thinking of a more conventional style of speciation‐focused Darwinism, which sometimes confuses process with result.     

Mechanistic and experimental analysis of condition and reproduction in a polymorphic lizard

Abstract The importance of genetic and environmental variation in condition in shaping evolutionary trade‐offs have recently been subject to much theoretical discussion, but is very difficult to investigate empirically in most field‐based systems. We present the results from mechanistic experimental manipulations of reproductive investment and condition in two female colour morphs (‘orange’ and ‘yellow’) of side‐blotched lizards (Uta stansburiana). We investigated the interactions between throat colour morphs, condition, local social environment and female survival using path‐analysis. Using follice‐ablation experiments, we show that large clutch size has a negative effect on field survival among yellow females, and that this effect is partly mediated by immunosuppressive effects of large clutches. In orange females these effects were less pronounced, and there was a negative survival effect of strong antibody responses. Hence, we experimentally confirmed our previous findings of correlational selection between female morphotype and immunocompetence, an important condition trait. Manipulation of corticosterone revealed multiple (‘pleiotropic’) direct and indirect effects of this hormone on both condition and reproductive traits. We argue that interaction effects (e.g. between local environments and genotypes) could explain a substantial fraction of variation in condition and reproduction in natural populations. Increased attention to such interaction effects and their fitness consequences will provide novel insights in field studies of selection and reproductive allocation.     

Population differentiation and evolution in the common guillemot Uria aalge

Common (Uria aalge) and Brünnich's guillemots (U. Iomvia) are colonial seabirds that nest in temperate to arctic oceans throughout the Northern hemisphere. They are very similar in the characteristics of ecology, demography and life history that are thought to determine the extent of differentiation among populations, yet geographic variation in morphology is notably greater in common guillemots. Despite evidence of strong natal philopatry, previous analyses of allozymes and the mitochondrial cytochrome b gene revealed little genetic differentiation among North Atlantic colonies of Brünnich's guillemots. To determine if the more extensive morphological variability in common guillemots reflects greater genetic variability, we sequenced part of the cytochrome b gene for 160 common guillemots from 10 colonies distributed throughout the Northern hemisphere. Genotype frequencies and phylogenetic relationships among genotypes both indicated that Atlantic and Pacific populations are genetically distinct. Genetic divergence among genotypes suggested that differentiation of these populations has resulted from separation by Pleistocene glaciers and the Bering Landbridge, as well as by currently unsuitable breeding habitat in the Arctic Ocean. Cytochrome b genotype frequencies also differed among Atlantic colonies, and appeared to define a cline similar to that described for morphological characters. Analyses of sequence variation suggested that this variation probably results from secondary contact between two refugial populations from the Pleistocene glaciations, rather than from isolation by distance or selection. In contrast, the Atlantic population of Brünnich's guillemots appears to have arisen through recent expansion of a single homogeneous refugial population.     

Adaptive divergence in plasticity in natural populations of Impatiens capensis and its consequences for performance in novel habitats

We tested for adaptive differentiation between two natural populations of Impatiens capensis from sites known to differ in selection on plasticity to density. We also determined the degree to which plasticity to density within a site was correlated with plastic responses of experimental immigrants to foreign sites. Inbred lines, derived from natural populations in an open-canopy site and a woodland site, were planted reciprocally in both original sites at naturally occurring high densities and at low density. The density manipulation represents environmental variation typically experienced within the site of a given population, and the transplant manipulation represents environmental differences between sites of different populations. Internode elongation, meristem allocation, leaf length, flowering date, and total lifetime fitness were measured. Genotypes originating in the open site, where selection favored plasticity of first internode length and flowering time (Donohue et al. 2000a), were more plastic in those characters than genotypes originating from the woodland site, where plasticity was maladaptive. Therefore, these two populations appear to have responded to divergent selection on plasticity. Plasticity to density strongly resembled plasticity to site differences for many characters, suggesting that similar environmental factors elicit plasticity both to density and to overhead canopy. Thus, plasticity that evolved in response to density variation within a site influenced phenotypic expression in the foreign site. Plastic responses to site caused immigrants from foreign populations to resemble native genotypes more closely. In particular, immigrants from the open site converged toward the selectively favored early-flowering phenotype of native genotypes in the woodland site, thereby reducing potential fitness differences between foreign and native genotypes. However, because genotypes from the woods population were less plastic than genotypes from the sun population, phenotypic differences between populations were greatest in the open site at low density. Therefore, population differences in plasticity can cause genotypes from foreign populations to be more strongly selected against in some environments than in others. However, genetic constraints and limits to plasticity prevented complete convergence of immigrants to the native phenotype in any environment.     

Genome‐wide differentiation in closely related populations: the roles of selection and geographic isolation

Population divergence in geographic isolation is due to a combination of factors. Natural and sexual selection may be important in shaping patterns of population differentiation, a pattern referred to as ‘isolation by adaptation’ (IBA). IBA can be complementary to the well‐known pattern of ‘isolation by distance’ (IBD), in which the divergence of closely related populations (via any evolutionary process) is associated with geographic isolation. The barn swallow Hirundo rustica complex comprises six closely related subspecies, where divergent sexual selection is associated with phenotypic differentiation among allopatric populations. To investigate the relative contributions of selection and geographic distance to genome‐wide differentiation, we compared genotypic and phenotypic variation from 350 barn swallows sampled across eight populations (28 pairwise comparisons) from four different subspecies. We report a draft whole‐genome sequence for H. rustica, to which we aligned a set of 9493 single nucleotide polymorphisms (SNPs). Using statistical approaches to control for spatial autocorrelation of phenotypic variables and geographic distance, we find that divergence in traits related to migratory behaviour and sexual signalling, as well as geographic distance, together explain over 70% of genome‐wide divergence among populations. Controlling for IBD, we find 42% of genomewide divergence is attributable to IBA through pairwise differences in traits related to migratory behaviour and sexual signalling alone. By (i) combining these results with prior studies of how selection shapes morphological differentiation and (ii) accounting for spatial autocorrelation, we infer that morphological adaptation plays a large role in shaping population‐level differentiation in this group of closely related populations.     

Unemployment,deindustrialization, and ‘community economy’ in eastern Germany

Drawing from an evening of fieldwork at an eastern German Protestant churchin the rapidly deindustrialized city of Leipzig, this article finalyzes a discussion among church leaders, former ‘dissidents,’ and unemployed workers on the subject of ‘community economy’ (Gemeinschaftsökonomie), a concept people interpret to represent a potential solution to the crisis of mass unemployment. Such local debates on unemployment offer a frame for understanding the re-negotiation of labor and social welfare in eastern Germany following socialism's end. finalyzing this discussion within the context of theoretical debates on ‘civil society,’ I follow Burawoy's and Gramsci's lead in fillustrating that the imagined economic sphere of ‘community economy’ is an ideological battle ground, where hegemonic discourse supporting economic neoliberalism may be either reinforced or subverted.     

中国猕猴生态学研究进展

中国的灵长类学研究始于19世纪中期之后,而兴盛于20世纪80年代至今。猕猴（Macaca mulatta）是世界及中国分布最为广泛的一种非人灵长类动物,在中国境内分布于17个省（市、区）,已被列为国家二级重点保护野生动物。迄今为止,学者们已对猕猴进行了包括地理分布、种群动态、食性、社会生态、保护生态等多方面的研究。本文拟对国内有关猕猴生态学方面的研究工作进行回顾与综述,以期通过对以往工作的汇总,梳理关于猕猴的研究线索与动态,并对今后的研究有所启示。     

Intragenomic conflict produces sex ratio dynamics that favor maternal sex ratio distorters

Maternal sex ratio distorters (MSDs) are selfish elements that enhance their transmission by biasing their host's sex allocation in favor of females. While previous models have predicted that the female‐biased populations resulting from sex ratio distortion can benefit from enhanced productivity, these models neglect Fisherian selection for nuclear suppressors, an unrealistic assumption in most systems. We used individual‐based computer simulation modeling to explore the intragenomic conflict between sex ratio distorters and their suppressors and explored the impacts of these dynamics on population‐level competition between species characterized by MSDs and those lacking them. The conflict between distorters and suppressors was capable of producing large cyclical fluctuations in the population sex ratio and reproductive rate. Despite fitness costs associated with the distorters and suppressors, MSD populations often exhibited enhanced productivity and outcompeted non‐MSD populations in single and multiple‐population competition simulations. Notably, the conflict itself is beneficial to the success of populations, as sex ratio oscillations limit the competitive deficits associated with prolonged periods of male rarity. Although intragenomic conflict has been historically viewed as deleterious to populations, our results suggest that distorter–suppressor conflict can provide population‐level advantages, potentially helping to explain the persistence of sex ratio distorters in a range of taxa.     

Genetic diversity analysis and conservation implications for the Iberian threatened populations of the irano-turanian relict Krascheninnikovia ceratoides (Chenopodiaceae)

Krascheninnikovia ceratoides (L.) Gueldenst. (Chenopodiaceae) is an irano‐turanian steppe plant with a striking geographical vicariance between the western Mediterranean and the central Asian regions. Its westernmost populations are located in the north‐east part of the Iberian Peninsula, in the narrow middle Ebro and Alfambra valleys, where they are threatened and have been catalogued as ‘vulnerable’. Genetic diversity and structure was studied in 150 individuals from five populations of these two valleys using inter‐simple sequence repeats (ISSR). A total of 121 informative bands allowed the identification of 150 genotypes. Nei's genetic diversity found in all natural populations (h = 0.448) was higher than that of other geographical restricted species. Analysis of molecular variance and spatial correlations analyses showed a strong genetic differentiation among populations (35.88%) and among valleys (22.33%). The unweighted pair‐group method of arithmetical averages and Neighbour‐joining clusterings further demonstrated a substructure of two population cores within the Ebro valley. Our genetic data suggest that the high levels of genetic diversity and the strong genetic structure found among the northern Iberian populations and ranges of K. ceratoides might result from the summed effects of its tetraploidy, its outbreeding nature, and its success in colonizing newly altered areas. However, the ISSR data might also reflect the existence of an ancient wider distribution range of the plant in the Iberian Peninsula coupled with a more recent history of habitat fragmentation. Different management conservation guidelines are recommended for this plant after our genetic analysis: a microreserve of approximately 2 km² is proposed for the highly threatened population of Osera (Ebro valley), whereas seed collection strategies and occasional population reinforcements are suggested for the remaining populations. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92 , 419–429.     

The effects of competition on the strength and softness of selection

Deleterious alleles are constantly introduced into populations due to mutation. In subdivided populations, the impact of these mutations depends on the strength of selection as well as the softness of selection, that is, the extent to which fitness is governed by local rather than global competition. It is widely appreciated that the intensity and type of competition will affect selection on deleterious mutations but most empirical work has focused solely on the effects of competition on selection strength. However, competition has rarely been studied in the context of selection ‘softness’ even though competition is at the conceptual root of soft selection. All other things being equal, theory predicts that inter‐ and intraspecific competitions have opposing effects on the softness of selection. Using Drosophila melanogaster, we estimated the strength and softness of selection in a ‘baseline’ competitive environment as well as two additional competitive environments characterized by either additional intra‐ or interspecific competitors. We found that competitive environment had little effect on the average strength of selection. While the softness of selection was affected by the type of competition, the direction of change varied across tests of different genes, contrary to expectation. Although the ‘hard/soft’ selection paradigm implicitly assumes that all individuals are equally sensitive to the local competitive environment, we found this not to be the case. Wild‐type individuals were more sensitive to changes in the genetic quality of their local competitors than mutant individuals.     

Between migration load and evolutionary rescue: dispersal,adaptation and the response of spatially structured populations to environmental change

The evolutionary potential of populations is mainly determined by population size and available genetic variance. However, the adaptability of spatially structured populations may also be affected by dispersal: positively by spreading beneficial mutations across sub-populations, but negatively by moving locally adapted alleles between demes. We develop an individual-based, two-patch, allelic model to investigate the balance between these opposing effects on a population''s evolutionary response to rapid climate change. Individual fitness is controlled by two polygenic traits coding for local adaptation either to the environment or to climate. Under conditions of selection that favour the evolution of a generalist phenotype (i.e. weak divergent selection between patches) dispersal has an overall positive effect on the persistence of the population. However, when selection favours locally adapted specialists, the beneficial effects of dispersal outweigh the associated increase in maladaptation for a narrow range of parameter space only (intermediate selection strength and low linkage among loci), where the spread of beneficial climate alleles is not strongly hampered by selection against non-specialists. Given that local selection across heterogeneous and fragmented landscapes is common, the complex effect of dispersal that we describe will play an important role in determining the evolutionary dynamics of many species under rapidly changing climate.     

Theodosius Dobzhansky and the genetic race concept

The use of ‘race’ as a proxy for population structure in the genetic mapping of complex traits has provoked controversy about its legitimacy as a category for biomedical research, given its social and political connotations. The controversy has reignited debates among scientists and philosophers of science about whether there is a legitimate biological concept of race. This paper examines the genetic race concept as it developed historically in the work of Theodosius Dobzhansky from the 1930s to 1950s. Dobzhansky’s definitions of race changed over this time from races as ‘arrays of forms’ or ‘clusters’ in 1933–1939, to races as genetically distinct geographical populations in 1940–1946, to races as genetically distinct ‘Mendelian populations’ in 1947–1955. Dobzhansky responded to nominalist challenges by appealing to the biological reality of race as a process. This response came into tension with the object ontology of race that was implied by Dobzhansky’s increasingly holistic treatment of Mendelian populations, a tension, the paper argues, he failed to appreciate or resolve.     

HIERARCHICAL GENETIC STRUCTURE AND GENE FLOW IN MACROGEOGRAPHIC POPULATIONS OF THE EASTERN TENT CATERPILLAR (MALACOSOMA AMERICANUM)

Genetic structure and inferred rates of gene flow in macrogeographic populations of the eastern tent caterpillar Malacosoma americanum were analyzed at two hierarchical scales: local demes and regional subpopulations. Wright's F-statistics were used to estimate population genetic structure using multilocus genotypic data generated electrophoretically. Estimated values of F_ST and the distribution of private alleles were then used to obtain indirect estimates of gene flow. We found modest, though significant, genetic structure at both spatial scales, a pattern consistent with high rates of gene flow over the large distances involved. Modest values obtained for Nei's genetic distance also suggested high levels of gene flow across the range of this species, although some gene-flow restriction resulting from isolation by distance was suggested by a positive regression of genetic distance on geographic distance. The observed homogeneity at enzyme loci across the range of M. americanum parallels the reported uniformity in morphology, suggesting a general absence of local genetic differentiation in this widely distributed species. The genetic homogeneity observed in this wide-ranging insect is discussed in terms of organism-specific environmental experience at different spatial scales. Some organisms occupying apparently heterogeneous environments may ameliorate unsuitable local conditions through microhabitat selection or behavioral modification of their microenvironment. This may be accomplished in M. americanum through group shelter construction and behavioral thermoregulation, closely tying thermoregulation to social biology in this species. If in this way the tent helps produce an effectively homogeneous environment for this species across its extensive range, this system may provide a unique example of how social behavior can influence the distribution of genetic variation in a population.     

How can we meet ‘the demands of the day’? Producing an affective,reflexive, interpretive,public sociology of ‘race’

This article argues for a public sociology of ‘race’ that can respond to Weber's injunction that sociology should ‘meet the demands of the day’. While the author's version of these demands – for a society of autonomous individuals and groups, living as equals – is utopian, the main argument offered here is that a sociology of ‘race’ should be a modified version of Burawoy's ‘public sociology’. Adopting Bauman's notion of a sociology of interpreters, a further suggestion is that this type of sociology needs to be reflexive and affective. Based on an analysis of his own sociological education in the late 1960s, his participation in social and political movements in which ‘race’ was key, and with brief reference to the sociology of ‘race’, the author argues that the emotions that circulated in each arena need to be examined, acknowledged and incorporated if theoretical and practical progress is to be made.