Evolution in an afternoon: rapid natural selection and adaptation of bacterial populations

This paper presents further findings from a study of young people's understanding of genetics towards the end of their compulsory science education. It focuses on the ability of these students to distinguish between genes and genetic information and the extent to which they are aware of the continuity of genetic information between cells within one individual. Many students hold the misconception that cells of different types will contain different genetic information because they have different functions and will therefore require different information. Confused, conflicting, and uncertain reasoning is also common. The implications of these findings in terms of understanding cell division are considered.     

Local adaptation in European populations of Arabidopsis lyrata (Brassicaceae)

We studied local adaptation to contrasting environments using an organism that is emerging as a model for evolutionary plant biology-the outcrossing, perennial herb Arabidopsis lyrata subsp. petraea (Brassicaceae). With reciprocal transplant experiments, we found variation in cumulative fitness, indicating adaptive differentiation among populations. Nonlocal populations did not have significantly higher fitness than the local population. Experimental sites were located in Norway (alpine), Sweden (coastal), and Germany (continental). At all sites after one year, the local population had higher cumulative fitness, as quantified by survival combined with rosette area, than at least one of the nonlocal populations. At the Norwegian site, measurements were done for two additional years, and fitness differences persisted. The fitness components that contributed most to differences in cumulative fitness varied among sites. Relatively small rosette area combined with a large number of inflorescences produced by German plants may reflect differentiation in life history. The results of the current study demonstrate adaptive population differentiation in A. lyrata along a climatic gradient in Europe. The studied populations harbor considerable variation in several characters contributing to adaptive population differentiation. The wealth of genetic information available makes A. lyrata a highly attractive system also for examining the functional and genetic basis of local adaptation in plants.     

Fluctuating asymmetry and allozymic heterozygosity among natural populations of pocket gophers (Thomomys bottae)

Fluctuating asymmetry, or random deviations from bilateral symmetry, has been widely used as a measure of developmental stability. The relationship between fluctuating asymmetry (FA) and allozymic heterozygosity was evaluated using 18 natural populations of pocket gophers ( Thomomys bottae ). Heterozygosity in local populations of pocket gophers ranges over more than an order of magnitude (1.5—18.4%), making this burrowing rodent particularly apt for such studies. Two measures of FA in mensural skull characters were examined: absolute deviations between left and right sides and the variance of signed differences. After log transformations, levels of FA among individuals and populations were not related to size. Repeated-measures analyses of variance showed that FA was significant relative to measurement error, both across populations and within them. Asymmetries of different characters were uncorrelated, despite positive significant correlations among the characters themselves. FA levels varied only slightly among populations of gophers, and this variation was not significant for most characters. FA levels of populations were not correlated with allozymic heterozygosity, and analyses of variance in FA employing heterozygosity were not significant. Heterozygosity levels in these rodents appear more strongly related to aspects of population history (especially effective size and gene flow) than to developmental stability. Because so many genomic and environmental factors can affect morphological variation, caution is needed in interpreting correlations between genetic and phenetic variation.     

Revision of Chaetodipus arenarius (Rodentia: Heteromyidae)

Chaetodipus arenarius is an endemic species of the Baja California Peninsula. It has undergone taxonomic changes in the last few years. Today, two species, C. arenarius and Chaetodipus dalquesti, are formally recognized with an unknown range for each. However, genetic analysis showed the possible presence of a third species. The objectives of this study were to use molecular data (cytochrome b and cytochrome c oxidase subunit III genes) to determine how many genetic groups are present in C. arenarius in the Baja California Peninsula; if these groups have morphological characteristics that could be used to distinguish them; if the genetic groups have limited distributions; identify taxonomic implications; and establish if there are any associations amongst genetic groups and different habitats. Bayesian inference, maximum parsimony, maximum likelihood, distance optimality criteria, and minimum spanning network indicated three monophyletic groups with high genetic differences (5.54–13.59%). These groups are morphologically diagnosable based on pelage and morphometric characters and geographical range. The three genetic groups correspond to three taxa previously described as subspecies or species. Based on our results, these should be considered to be different species: C. arenarius occupies the most extreme habitats with hot summers; C. dalquesti occupies the moistest coastal areas in the southern part of the peninsula, and Chaetodipus siccus is restricted by mountain ranges to the isolated Los Planes Basin and Cerralvo Island. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010.     

Footprints of divergent selection in natural populations of Castanopsis fargesii (Fagaceae)

Given predicted rapid climate change, an understanding of how environmental factors affect genetic diversity in natural populations is important. Future selection pressures are inherently unpredictable, so forest management policies should maintain both overall diversity and identify genetic markers associated with the environmental factors expected to change most rapidly, like temperature and rainfall. In this study, we genotyped 648 individuals in 28 populations of Castanopsis fargesii (Fagaceae) using 32 expressed sequence tag (EST)-derived microsatellite markers. After removing six loci that departed from Hardy–Weinberg equilibrium, we measured genetic variation, population structure and identified candidate loci putatively under selection by temperature and precipitation. We found that C. fargesii populations possessed high genetic diversity and moderate differentiation among them, indicating predominant outcrossing and few restrictions to gene flow. These patterns reduce the possible impact of stochastic effects or the influence of genetic isolation. Clear footprints of divergent selection at four loci were discovered. Frequencies of five alleles at these loci were strongly correlated with environmental factors, particularly extremes in precipitation. These alleles varied from being near fixation at one end of the gradient to being completely absent at the other. Our study species is an important forest tree in the subtropical regions of China and could have a major role in future management and reforestation plans. Our results demonstrate that the gene flow is widespread and abundant in natural populations, maintaining high diversity, while diversifying selection is acting on specific genomic regions.     

Different genes underlie adaptive melanism in different populations of rock pocket mice

Identifying the genes responsible for adaptation has been an elusive goal in evolutionary biology. Rock pocket mice (Chaetodipus intermedius) provide a useful system for studying the genetics of adaptation: most C. intermedius are light-coloured and live on light-coloured rocks, but in several different geographical regions, C. intermedius are melanic and live on dark-coloured basalt lava, presumably as an adaptation for crypsis. Previous work demonstrated that mutations at the melanocortin-1 receptor gene (Mc1r) are responsible for the dark/light difference in mice from one population in Arizona. Here, we investigate whether melanism has evolved independently in populations of dark C. intermedius from New Mexico, and whether the same or different genes underlie the dark phenotype in mice from these populations compared with the dark mice from Arizona. Seventy-six mice were collected from pairs of dark and light localities representing four different lava flows and adjacent light-coloured rocks; lava flows were separated by 70-750 km. Spectrophotometric analysis of mouse pelage and of rock samples revealed a strong positive association between coat colour and substrate colour. No significant differences were observed in the colour of rocks among the four lava flows, suggesting that mice in these separate populations have experienced similar selection for crypsis. Despite this similarity in environment, melanic mice from the three New Mexico populations were slightly, but significantly, darker than melanic mice from Arizona. The entire Mc1r gene was sequenced in all mice. The previously identified mutations responsible for the light/dark difference in mice from Arizona were absent in all melanic mice from three different populations in New Mexico. Five new Mc1r polymorphisms were observed among mice from New Mexico, but none showed any association with coat colour. These results indicate that adaptive melanism has arisen at least twice in C. intermedius and that these similar phenotypic changes have a different genetic basis.     

Macroevolution of life‐history traits in passerine birds: adaptation and phylogenetic inertia

We used a recent passerine phylogeny and comparative method to evaluate the macroevolution of body and egg mass, incubation and fledging periods, time to independence and time with parents of the main passerine lineages. We hypothesised that passerine reproductive traits are affected by adaptation to both past and present environmental factors and phenotypic attributes such as body mass. Our results suggest that the evolution of body and egg mass, time to independence, incubation and fledging times are affected by strong phylogenetic inertia and that these breeding traits are all affected by body mass. Time with parents, where major lineages exhibit their own fixed optima and body mass does not have an effect, and clutch size which is affected by body mass and additionally by climate regimes, do not exhibit any phylogenetic inertia.     

Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis)

The traditional view of the species as the fundamental unit of evolution has been challenged by observations that in heterogeneous environments, gene flow may be too restricted to overcome the effects of local selection. Whether a species evolves as a cohesive unit depends critically on the dynamic balance between homogenizing gene flow among populations and potentially disruptive local adaptation. To examine this evolutionary balance between "global" gene flow and local selection, we studied northern Californian populations of Helianthus exilis, the serpentine sunflower, within a mosaic of contrasting serpentine and nonserpentine areas that differ considerably in soil chemistry and water availability. Local adaptation to riparian and serpentine habitats was studied in Helianthus exilis along with an analysis of gene flow patterns among populations within these habitats. Local adaptation was assessed in H. exilis during 2002 and 2003 using reciprocal transplant experiments at multiple locations within serpentine and riparian habitats. Effects of competition and germination date on the expression of local adaptation were also examined within the reciprocal transplant experiments. Local adaptation was detected in both years at the local site level and at the level of habitat. The analysis of the transplanted populations indicated that the patterns of selection differed considerably between riparian and serpentine sites. Differential survivorship occurred in serpentine habitats, whereas selection on reproductive output predominated in riparian habitats. Local adaptation was expressed only in the absence of competition. Local adaptation in terms of survivorship was most strongly expressed in treatments with delayed seed germination. Microsatellite markers were used to quantify population genetic parameters and examine the patterns of gene flow among sampled populations. Analysis of molecular markers revealed a system of population patches that freely exchange genes with each other. Strong selection seems to maintain ecotypic variation within this endemic sunflower species, while extensive gene flow among populations prevents local speciation between serpentine and riparian ecotypes.     

Local adaptation of sex induction in a facultative sexual crustacean: insights from QTL mapping and natural populations of Daphnia magna

Dormancy is a common adaptation in invertebrates to survive harsh conditions. Triggered by environmental cues, populations produce resting eggs that allow them to survive temporally unsuitable conditions. Daphnia magna is a crustacean that reproduces by cyclical parthenogenesis, alternating between the production of asexual offspring and the sexual reproduction of diapausing eggs (ephippia). Prior to ephippia production, males (necessary to ensure ephippia fertilization) are produced parthenogenetically. Both the production of ephippia and the parthenogenetic production of males are induced by environmental factors. Here, we test the hypothesis that the induction of D. magna resting egg production shows a signature of local adaptation. We postulated that Daphnia from permanent ponds would produce fewer ephippia and males than Daphnia from intermittent ponds and that the frequency and season of habitat deterioration would correlate with the timing and amount of male and ephippia production. To test this, we quantified the production of males and ephippia in clonal D. magna populations in several different controlled environments. We found that the production of both ephippia and males varies strongly among populations in a way that suggests local adaptation. By performing quantitative trait locus mapping with parent clones from contrasting pond environments, we identified nonoverlapping genomic regions associated with male and ephippia production. As the traits are influenced by two different genomic regions, and both are necessary for successful resting egg production, we suggest that the genes for their induction co‐evolve.     

The geometry of natural selection in cave and spring populations of the amphipod Gammarus minus Say (Crustacea: Amphipoda)

The shape of the fitness function was investigated in a spring population (Davis Spring) and a cave population (Organ Cave) of the amphipod Gammarus minus in southern West Virginia. The first three principal components of a series of size, antennal and eye measurements and two fitness components (amplexus and number of eggs) were investigated. Smoothing splines using generalized cross-validation scores were found as were least-squares quadratic regression equations. Confidence intervals on shape, as determined by a smoothing parameter, were calculated using a bootstrap approach. Out of 18 cases, there were six cases of no selection, six cases of directional (monotonic) selection, one case of stabilizing selection, one case of disruptive selection, and four cases of selection with multiple internal maxima and minima. Selection on the cave population was frequently directional (5), resulting from strong directional selection for increased size, larger antennae, and smaller eyes. Selection on the spring population, the ancestral habitat for the species, was frequently non-monotonic (five cases) and rarely directional (one case). In both populations, stabilizing selection was rare and no more common than disruptive selection.     

The genetic consequences of selection in natural populations

The selection coefficient, s, quantifies the strength of selection acting on a genetic variant. Despite this parameter's central importance to population genetic models, until recently we have known relatively little about the value of s in natural populations. With the development of molecular genetic techniques in the late 20th century and the sequencing technologies that followed, biologists are now able to identify genetic variants and directly relate them to organismal fitness. We reviewed the literature for published estimates of natural selection acting at the genetic level and found over 3000 estimates of selection coefficients from 79 studies. Selection coefficients were roughly exponentially distributed, suggesting that the impact of selection at the genetic level is generally weak but can occasionally be quite strong. We used both nonparametric statistics and formal random‐effects meta‐analysis to determine how selection varies across biological and methodological categories. Selection was stronger when measured over shorter timescales, with the mean magnitude of s greatest for studies that measured selection within a single generation. Our analyses found conflicting trends when considering how selection varies with the genetic scale (e.g., SNPs or haplotypes) at which it is measured, suggesting a need for further research. Besides these quantitative conclusions, we highlight key issues in the calculation, interpretation, and reporting of selection coefficients and provide recommendations for future research.     

The strength of phenotypic selection in natural populations

How strong is phenotypic selection on quantitative traits in the wild? We reviewed the literature from 1984 through 1997 for studies that estimated the strength of linear and quadratic selection in terms of standardized selection gradients or differentials on natural variation in quantitative traits for field populations. We tabulated 63 published studies of 62 species that reported over 2,500 estimates of linear or quadratic selection. More than 80% of the estimates were for morphological traits; there is very little data for behavioral or physiological traits. Most published selection studies were unreplicated and had sample sizes below 135 individuals, resulting in low statistical power to detect selection of the magnitude typically reported for natural populations. The absolute values of linear selection gradients |beta| were exponentially distributed with an overall median of 0.16, suggesting that strong directional selection was uncommon. The values of |beta| for selection on morphological and on life-history/phenological traits were significantly different: on average, selection on morphology was stronger than selection on phenology/life history. Similarly, the values of |beta| for selection via aspects of survival, fecundity, and mating success were significantly different: on average, selection on mating success was stronger than on survival. Comparisons of estimated linear selection gradients and differentials suggest that indirect components of phenotypic selection were usually modest relative to direct components. The absolute values of quadratic selection gradients |gamma| were exponentially distributed with an overall median of only 0.10, suggesting that quadratic selection is typically quite weak. The distribution of gamma values was symmetric about 0, providing no evidence that stabilizing selection is stronger or more common than disruptive selection in nature.     

Spatio-temporal variation of natural and sexual selection in breeding populations of the coreid bug,Colpula lativentris (Heteroptera: Coreidae)

Spatio-temporal variations of lifetime reproductive succes (LRS) of both male and female individuals of a coreid bugColpula lativentris were measured and analyzed using the multiple regression method of Arnold and Wade (1984a, b). The standardized variance of LRS was larger in males than that in females as males often to secure mates for a long period whereas females could easily find mates and oviposit simply dependent on ovarial maturation. LRS was partitioned into 4 consecutive fitness components: (1) reproductive lifespan, (2) copulating efficiency, (3) guarding efficiency (for males) or oviposition efficiency (for females), and (4) number of eggs per clutch. In males copulating efficiency was the largest determining factor of LRS, whereas in females reproductive lifespan was the most important factor. Such tendencies were stable on both a yearly and local basis. Patterns of relative contribution of natural selection (reproductive lifespan and number of eggs per clutch) and sexual selection (copulating efficiency and guarding or oviposition efficiency) to LRS were clearly different between males and females. This sexual difference is, at least to some extent, thought to be brought about by sexual selection among males for mating opportunity, though no physical fight was observed among males. Directional selection on body length was found only in relation to the clutch size of females because large females tended to lay larger clutches. No significant directional selection was found in other fitness components.     

On the rate of genetic adaptation under natural selection.

Unsaturated fatty acids are constituents of nearly all biological membranes. They are always present in membranes which possess transmembrane potentials. Two completely different biosynthetic routes have evolved (aerobic and anaerobic) for placing cis double bonds in the 9 position on the fatty acids of membrane lipids. Bacterial membranes contain primarily monounsaturated fatty acids, whereas eukaryote membranes contain a significant fraction of polyunsaturated fatty acids. The polyunsaturated fatty acids are concentrated in organelles, such as chloroplasts and mitochondria that are known to manipulate transmembrane potentials. I propose that the function of the unsaturated fatty acids is to facilitate the transmission of a local compaction of the membrane (in response to a transmembrane potential) laterally through the membrane. The role of the cis double bond at position 9 is twofold: first to create a kink in the chains of a large fraction of membrane fatty acids enhancing the separation of two regions in the membrane and second to enhance the rigidity of the membrane in the region between the head group and the 9 double bond. This ordered region contains those carbons proximal to the 9 carbon and which are in a regular array of trans conformations. The presence of a reasonable proportion of cis double bonds at position 9 will tend to maintain these trans conformations utilizing pi-pi (van der Waals) interactions between adjacent hydrocarbon chains at position 9. The disordered region contains the carbons distal to the 9 carbon. These have greater degrees of freedom and considerable gauche conformations. The role of the double bonds in the polyunsaturated fatty acids distal to carbon 9 is to facilitate trans bilayer pi-pi (van der Waals) interactions enhancing compaction of the bilayer during the electrostriction. I further propose that it is the function of the ionic headgroups to form an interlocking polyionic network which constitutes an elastic sheet. These ionic interactions would serve as the restoring force converting the compaction into a wave. The facilitation of the compaction of the bilayer together with the polyionic restoring force permits the membrane to transmit conformational changes from one transmembrane protein to another. Since transmembrane potentials are created and responded to by proteins each in a single location, it is thus proposed that a potential compaction wave emanates from the first protein in all directions in the plane of the membrane. The proposed wave would have both physical and electrical components. The electrohydrodynamic wave would require that the compaction oscillations be coupled to an oscillating electrical field. These proposals are applied to mitochondrial oxidative phosphorylation, and to transport across biological membranes.     

Phenotypic variation in Galerida larks in Morocco: the role of history and natural selection

The relative influences of history, natural selection and hybridization in shaping phenotypic variation in closely related taxa is a crucial issue in current evolutionary biology. In this study, we used as a model two sibling but paradoxically highly variable species of larks (Galerida theklae and Galerida cristata) of Morocco to separate the impacts of these evolutionary forces. In the former species, variation is manifested mainly in colouration, while in the latter, variation also encompasses bill size and shape. Mitochondrial and nuclear DNA sequencing were used to identify the historical relationships among the subspecies and species. According to our analyses, G. cristata and G. theklae diverged about 3.7 million years ago (Ma), and we found no evidence for a role of hybridization in maintaining their similarity. In G. theklae, there was no further subdivision, while in G. cristata two major mtDNA groups were identified (divergence approximately 1.1 Ma). These two lineages are parapatric and regroup, respectively, the three short-billed subspecies [G. (cristata) cristata] and the two long-billed subspecies [G. (cristata) randonii]. Patterns of morphological variation were then contrasted to this pattern of neutral relationships: we found that G. (c.) cristata was morphologically more similar to G. theklae than to G. (c.) randonii. Overall, these results point towards the prominent role of (i) natural selection and/or phenotypic plasticity in adapting the plumage to local conditions and (ii) natural selection in combination with historical isolation in driving the divergence in size and bill morphology in the crested larks.     

Secondary theorem of natural selection in biocultural populations.

The "Secondary Theorem of Natural Selection," an extension of Fisher's fundamental theorem, states that the rate of change in the mean of an arbitrary character in response to selection is proportional to the additive genetic covariance between the character and fitness. Here I derive an expression for the change in the mean value of a trait subject to both genetic and cultural transmission. I start with the one-locus case under generalized mating and cultural transmission from parents to offspring, then proceed to the two-locus case. My results support previous work on the effects of nongenetic inheritance by showing that (i) cultural transmission introduces a timelag in the population response to selection; (ii) with cultural transmission the effects of selection persist even after selection is relaxed; and (iii) cultural transmission can either enhance or retard phenotypic evolution relative to that obtained under purely genetic transmission.     

Habitat-specific natural selection at a flowering-time QTL is a main driver of local adaptation in two wild barley populations

Understanding the genetic basis of local adaptation requires insight in the fitness effects of individual loci under natural field conditions. While rapid progress is made in the search for genes that control differences between plant populations, it is typically unknown whether the genes under study are in fact key targets of habitat-specific natural selection. Using a quantitative trait loci (QTL) approach, we show that a QTL associated with flowering-time variation between two locally adapted wild barley populations is an important determinant of fitness in one, but not in the other population's native habitat. The QTL mapped to the same position as a habitat-specific QTL for field fitness that affected plant reproductive output in only one of the parental habitats, indicating that the genomic region is under differential selection between the native habitats. Consistent with the QTL results, phenotypic selection of flowering time differed between the two environments, whereas other traits (growth rate and seed weight) were under selection but experienced no habitat-specific differential selection. This implies the flowering-time QTL as a driver of adaptive population divergence. Our results from phenotypic selection and QTL analysis are consistent with local adaptation without genetic trade-offs in performance across environments, i.e. without alleles or traits having opposing fitness effects in contrasting environments.