QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. II. ANALYSIS OF SELECTION AND RANDOM CHANGE IN FOSSIL SPECIES USING RECONSTRUCTED GENETIC PARAMETERS

The roles of natural selection and random genetic change in the punctuated phenotypic evolution of eight Miocene-Pliocene tropical American species of the cheilostome bryozoan Metrarabdotos are analyzed by quantitative genetic methods. Trait heritabilities and genetic covariances reconstructed by partitioning within- and among-colony phenotypic variance are similar to those previously obtained for living species of the cheilostome Stylopoma using breeding data. The hypothesis that differences in skeletal morphology between species of Metrarabdotos are entirely due to mutation and genetic drift cannot be rejected for reasonable rates of mutation maintained for periods brief enough to account for the geologically abrupt appearances of these species in the fossil record. Except for one pair of species, separated by the largest morphologic distance, directional selection acting alone would require unrealistically high rates of selective mortality to be maintained for these periods. Thus, directional selection is not strongly implicated in the divergence of Metrarabdotos species. Within species, rates of net phenotypic change are slow enough to require stabilizing selection, but mask large, relatively rapid fluctuations, all of which, however, can be attributed to chance departures from the mean phenotype by mutation and genetic drift, rather than to tracking environmental fluctuation by directional selection. The results are consistent with genetic models involving shifts between multiple adaptive peaks on which phenotypes remain more or less static through long-term stabilizing selection. Regardless of the degree to which directional selection may be involved in peak shifts, phenotypic differentiation is thus related to processes different than the pervasive stabilizing selection acting within species.     

Observing populations and testing predictions about genetic drift in a computer simulation improves college students’ conceptual understanding

Background

Evolution is a difficult subject for students, with well-documented confusion about natural selection, tree thinking, and genetic drift among other topics. Here we investigate the effect of a simulation-based module about the conservation of black-footed ferrets, a module designed with pedagogical approaches that have been demonstrated to be effective, for teaching genetic drift. We compared performance on the Genetic Drift Inventory (GeDI) of students who completed the module and students who were in classes that used other methods for teaching genetic drift.

Results

Students in 19 courses using the simulation-based module improved their understanding of genetic drift significantly after completing the Ferrets module, as measured by the GeDI. Students in five control courses actually performed significantly worse on the GeDI after instruction. The lower scores in the control courses were driven by a decrease in these students’ understanding of key concepts.

Conclusions

The Ferrets module appears to be an effective way to teach genetic drift. In the control courses, students’ progress in understanding genetic drift may pass through a stage where their understanding of key concepts is worse than it was prior to instruction. However, students who learned genetic drift in courses that used the Ferrets module showed a more rapid increase in their understanding of key concepts related to genetic drift. This result suggests that the paths that students can take to move from novice to expert understanding may be more varied than was previously predicted.

     

DOES MATE LIMITATION IN SELF‐INCOMPATIBLE SPECIES PROMOTE THE EVOLUTION OF SELFING? THE CASE OF LEAVENWORTHIA ALABAMICA

Genetic diversity at the S‐locus controlling self‐incompatibility (SI) is often high because of negative frequency‐dependent selection. In species with highly patchy spatial distributions, genetic drift can overwhelm balancing selection and cause stochastic loss of S‐alleles. Natural selection may favor the breakdown of SI in populations with few S‐alleles because low S‐allele diversity constrains the seed production of self‐incompatible plants. We estimated S‐allele diversity, effective population sizes, and migration rates in Leavenworthia alabamica, a self‐incompatible mustard species restricted to discrete habitat patches in rocky glades. Patterns of polymorphism were investigated at the S‐locus and 15 neutral microsatellites in three large and three small populations with 100‐fold variation in glade size. Populations on larger glades maintained more S‐alleles, but all populations were estimated to harbor at least 20 S‐alleles, and mate availabilities typically exceeded 0.80, which is consistent with little mate limitation in nature. Estimates of the effective size (N_e) in each population ranged from 600 to 1600, and estimated rates of migration (m) ranged from 3 × 10⁻⁴ to nearly 1 × 10⁻³. According to theoretical models, there is limited opportunity for genetic drift to reduce S‐allele diversity in populations with these attributes. Although pollinators or resources limit seed production in small glades, limited S‐allele diversity does not appear to be a factor promoting the incipient breakdown of SI in populations of this species that were studied.     

??Are Humans Evolving??? A Classroom Discussion to Change Student Misconceptions Regarding Natural Selection

Natural selection is an important mechanism in the unifying biological theory of evolution, but many undergraduate students struggle to learn this concept. Students enter introductory biology courses with predictable misconceptions about natural selection, and traditional teaching methods, such as lecturing, are unlikely to dispel these misconceptions. Instead, students are more likely to learn natural selection when they are engaged in instructional activities specifically designed to change misconceptions. Three instructional strategies useful for changing student conceptions include (1) eliciting na?ve conceptions from students, (2) challenging nonscientific conceptions, and (3) emphasizing conceptual frameworks throughout instruction. In this paper, we describe a classroom discussion of the question “Are humans evolving?” that employs these three strategies for teaching students how natural selection operates. Our assessment of this activity shows that it successfully elicits students’ misconceptions and improves student understanding of natural selection. Seventy-eight percent of our students who began this exercise with misconceptions were able to partially or completely change their misconceptions by the end of this discussion. The course that this activity was part of also showed significant learning gains (d = 1.48) on the short form of the Conceptual Inventory of Natural Selection. This paper includes all the background information, data, and visual aids an instructor will need to implement this activity.     

Evolution of migration under kin selection and local adaptation

We present here a stochastic two-locus, two-habitat model for the evolution of migration with local adaptation and kin selection. One locus determines the migration rate while the other causes local adaptation. We show that the opposing forces of kin competition and local adaptation can lead to the existence of one or two convergence stable migration rates, notably depending on the recombination rate between the two loci. We show that linkage between migration and local adaptation loci has two antagonist effects: when linkage is tight, cost of local adaptation increases, leading to smaller equilibrium migration rates. However, when linkage is tighter, the population structure at the migration locus tends to be very high because of the indirect selection, and thus equilibrium migration rates increases. This result, qualitatively different from results obtained with other models of migration evolution, indicates that ignoring drift or the detail of the genetic architecture may lead to incorrect conclusions.     

Sex and destiny: The role of mating signals in speciation and macroevolution

A growing body of research posits a central role for mating signals in speciation and the reproductive isolation of species, yet there has been relatively little consideration of mating signal evolution within macroevolutionary theory. Factors that influence the divergence of fertilization systems generally, and mating signals specifically, may incidentally influence rates of speciation and patterns of species sorting. Potential key processes include: genetic drift, natural selection (differential survival), selection for mate recognition, and sexual selection. This paper explores the integration of mating signal evolution into macroevolution and hierarchy theory, arguing that speciational patterns may frequently result from “effect sorting”; in which microevolutionary processes operating at the organismal level have macroevolutionary effects at the clade level. Preliminary evidence indicates that sexual selection is a widespread and potent evolutionary force that, together with other mechanisms, may have a large, though incidental impact on species sorting. The Mate Competition Hypothesis is here proposed to account for this possibility, postulating that heritable, clade‐specific variations in the intensity of sexual selection and the potential breadth of signal‐receiver systems contribute to divergent patterns of species‐richness. Several examples from the vertebrate fossil record are consistent with this hypothesis.     

Gryphaea and cepaea—case studies for teaching selection

An approach to the teaching of natural selection in evolution using materials related to living creatures instead of artificial models such as toothpicks is described. Some investigations using simple flow tanks to investigate the stability of Gryphaea shells and a simulated non-visual searching for Cepaea are suggested for use in class practical sessions. All the designs for the investigations suggested have been tested with students and found to be workable in the relatively short practical periods available for school sixth-form and College of Education students.     

learnPopGen: An R package for population genetic simulation and numerical analysis

Here, I briefly present a new R package called learnPopGen that has been designed primarily for the purposes of teaching evolutionary biology, population genetics, and evolutionary theory. Functions of the package can be used to conduct simulations and numerical analyses of a wide range of evolutionary phenomena that would typically be covered in advanced undergraduate through graduate‐level curricula in population genetics or evolution. For instance, learnPopGen functions can be used to visualize gene frequency changes through time under multiple deterministic and stochastic processes, to compute and animate the changes in phenotypic trait values or distributions under natural selection, to numerically analyze and graph the outcome of simple game theory models, and to plot coalescence within a population experiencing genetic drift, along with a number of other things. Functions have been designed to be maximally didactic and frequently employ compelling animated visualizations. Furthermore, it is straightforward to export plots and animations from R in the form of flat or animated graphics, or as videos. For maximum flexibility, students working with the package can run functions directly in R; however, instructors may choose to guide students less adept in the R environment to one of various web interfaces that I have built for a number of the functions of the package and that are already available online.     

Drift sometimes dominates selection,and vice versa: a reply to Clatterbuck,Sober and Lewontin

Clatterbuck et al. (Biol Philos 28: 577–592, 2013) argue that there is no fact of the matter whether selection dominates drift or vice versa in any particular case of evolution. Their reasons are not empirically based; rather, they are purely conceptual. We show that their conceptual presuppositions are unmotivated, unnecessary and overly complex. We also show that their conclusion runs contrary to current biological practice. The solution is to recognize that evolution involves a probabilistic sampling process, and that drift is a deviation from probabilistic expectation. We conclude that conceptually, there are no problems with distinguishing drift from selection, and empirically—as modern science illustrates—when drift does occur, there is a quantifiable fact of the matter to be discovered.     

Evolution in metacommunities

A metacommunity can be defined as a set of communities that are linked by migration, and extinction and recolonization. In metacommunities, evolution can occur not only by processes that occur within communities such as drift and individual selection, but also by among-community processes, such as divergent selection owing to random differences among communities in species composition, and group and community-level selection. The effect of these among-community-level processes depends on the pattern of migration among communities. Migrating units may be individuals (migrant pool model), groups of individuals (single-species propagule pool model) or multi-species associations (multi-species propagule pool model). The most interesting case is the multi-species propagule pool model. Although this pattern of migration may a priori seem rare, it becomes more plausible in small well-defined 'communities' such as symbiotic associations between two or a few species. Theoretical models and experimental studies show that community selection is potentially an effective evolutionary force. Such evolution can occur either through genetic changes within species or through changes in the species composition of the communities. Although laboratory studies show that community selection can be important, little is known about how important it is in natural populations.     

Selection never dominates drift (nor vice versa)

The probability that the fitter of two alleles will increase in frequency in a population goes up as the product of N (the effective population size) and s (the selection coefficient) increases. Discovering the distribution of values for this product across different alleles in different populations is a very important biological task. However, biologists often use the product Ns to define a different concept; they say that drift “dominates” selection or that drift is “stronger than” selection when Ns is much smaller than some threshold quantity (e.g., ½) and that the reverse is true when Ns is much larger than that threshold. We argue that the question of whether drift dominates selection for a single allele in a single population makes no sense. Selection and drift are causes of evolution, but there is no fact of the matter as to which cause is stronger in the evolution of any given allele.     

The adaptive value of epigenetic mutation: Limited in large but high in small peripheral populations

The fate of populations during range expansions, invasions and environmental changes is largely influenced by their ability to adapt to peripheral habitats. Recent models demonstrate that stable epigenetic modifications of gene expression that occur more frequently than genetic mutations can both help and hinder adaptation in panmictic populations. However, these models do not consider interactions between epimutations and evolutionary forces in peripheral populations. Here, we use mainland–island mathematical models and simulations to explore how the faster rate of epigenetic mutation compared to genetic mutations interacts with migration, selection and genetic drift to affect adaptation in peripheral populations. Our model focuses on cases where epigenetic marks are stably inherited. In a large peripheral population, where the effect of genetic drift is negligible, our analyses suggest that epimutations with random fitness impacts that occur at rates as high as 10^–3 increase local adaptation when migration is strong enough to overwhelm divergent selection. When migration is weak relative to selection and epimutations with random fitness impacts decrease adaptation, we find epigenetic modifications must be highly adaptively biased to enhance adaptation. Finally, in small peripheral populations, where genetic drift is strong, epimutations contribute to adaptation under a wider range of evolutionary conditions. Overall, our results suggest that epimutations can change outcomes of adaptation in peripheral populations, which has implications for understanding conservation and range expansions and contractions, especially of small populations.     

Beads and Dice in a Genetic Drift Exercise

Natural selection driving adaptive changes is a powerful and intuitive explanation for the evolution of the living world around us. Evolution at the molecular level, however, is chiefly ruled by random genetic drift. The idea that an advantageous allele may be lost by chance in a natural population is rather difficult to explore in the classroom. Low-cost and hands-on educational resources are needed to make genetic drift more intuitive among students. In this exercise, we use colored beads and the roll of a die to simulate drift and selection jointly affecting the fate of the genetic variants in an evolving population. Our aim is to teach students that natural selection does not determine but simply influences the fate of advantageous alleles because random genetic drift is always present. We have been using this exercise successfully for over a decade for the Biological Sciences students at the Federal University of Rio de Janeiro.     

Students’ Mental Models of Evolutionary Causation: Natural Selection and Genetic Drift

In an effort to understand how to improve student learning about evolution, a focus of science education research has been to document and address students?? naive ideas. Less research has investigated how students reason about alternative scientific models that attempt to explain the same phenomenon (e.g., which causal model best accounts for evolutionary change?). Within evolutionary biology, research has yet to explore how non-adaptive factors are situated within students?? conceptual ecologies of evolutionary causation. Do students construct evolutionary explanations that include non-adaptive and adaptive factors? If so, how are non-adaptive factors structured within students?? evolutionary explanations? We used clinical interviews and two paper and pencil instruments (one open-response and one multiple-choice) to investigate the use of non-adaptive and adaptive factors in undergraduate students?? patterns of evolutionary reasoning. After instruction that included non-adaptive causal factors (e.g., genetic drift), we found them to be remarkably uncommon in students?? explanatory models of evolutionary change in both written assessments and clinical interviews. However, consistent with many evolutionary biologists?? explanations, when students used non-adaptive factors they were conceptualized as causal alternatives to selection. Interestingly, use of non-adaptive factors was not associated with greater understanding of natural selection in interviews or written assessments, or with fewer naive ideas of natural selection. Thus, reasoning using non-adaptive factors appears to be a distinct facet of evolutionary thinking. We propose a theoretical framework for an expert?Cnovice continuum of evolutionary reasoning that incorporates both adaptive and non-adaptive factors, and can be used to inform instructional efficacy in evolutionary biology.     

Molecular evolution modeled as a fractal Poisson process in agreement with mammalian sequence comparisons

The fractal doubly stochastic Poisson process (FDSPP) model of molecular evolution, like other doubly stochastic Poisson models, agrees with the high estimates for the index of dispersion found from sequence comparisons. Unlike certain previous models, the FDSPP also predicts a positive geometric correlation between the index of dispersion and the mean number of substitutions. Such a relationship is statistically proven herein using comparisons between 49 mammalian genes. There is no characteristic rate associated with molecular evolution according to this model, but there is a scaling relationship in rates according to a fractal dimension of evolution. The FDSPP is a suitable replacement for the homogeneous Poisson process in tests of the lineage dependence of rates and in estimating confidence intervals for divergence times. As opposed to other fractal models, this model can be interpreted in terms of Darwinian selection and drift.      

Evolution at a multiallelic locus under migration and uniform selection

The semilinear parabolic system that describes the evolution of the gene frequencies in the diffusion approximation for migration and selection at a multiallelic locus is investigated. The population occupies a finite habitat of arbitrary dimensionality and shape. The drift and diffusion coefficients may depend on position, but the selection coefficients do not. It is established that if p is a uniform equilibrium point under pure selection, then p is a migration-selection equilibrium, and that generically the introduction of migration does not change the stability of p. It is also proved that if p is a uniform, globally asymptotically stable, internal equilibrium point under pure selection, then the gene frequencies converge to p when both migration and selection are present. Thus, in this case, after a sufficiently long time, there is no genetic indication of the spatial distribution of the population.     

A two-stage model for Cepaea polymorphism

The history of the study of snails in the genus Cepaea is briefly outlined. Cepaea nemoralis and C. hortensis are polymorphic for genetically controlled shell colour and banding, which has been the main interest of the work covered. Random drift, selective predation and climatic selection, both at a macro- and micro-scale, all affect gene frequency. The usual approach to understanding maintenance of the polymorphism, has been to look for centripetal effects on frequency. Possible processes include balance of mutation pressure and drift, heterozygote advantage, relational balance heterosis, frequency-dependent predation, multi-niche selective balance, or some combination of these. Mutational balance is overlaid by more substantial forces. There is some evidence for heterosis. Predation by birds may protect the polymorphism, and act apostatically to favour distinct morphs. Although not substantiated for Cepaea, many studies show that predators behave in the appropriate manner, while shell colour polymorphisms in molluscs occur most commonly in species exposed to visually searching predators. It is not known whether different thermal properties of the shells help to generate equilibria. Migration between colonies is probably greater than originally thought. The present geographical range has been occupied for less than 5000 generations. Climatic and human modification alter snail habitats relatively rapidly, which in turn changes selection pressures. A simple simulation shows that migration coupled with selection which fluctuates but is not centripetal, may retain polymorphism for sufficiently long to account for the patterns we see today. There may therefore be a two-stage basis to the polymorphism, comprising long-term but weak balancing forces coupled with fluctuating selection which does not necessarily balance but results in very slow elimination. Persistence of genetic variants in this way may provide the conditions for evolution of a balanced genome.     

DRIFT PROMOTES SPECIATION BY SEXUAL SELECTION

Quantitative genetic models of sexual selection have generally failed to provide a direct connection to speciation and to explore the consequences of finite population size. The connection to speciation has been indirect because the models have treated only the evolution of male and female traits and have stopped short of modeling the evolution of sexual isolation. In this article we extend Lande's (1981) model of sexual selection to quantify predictions about the evolution of sexual isolation and speciation. Our results, based on computer simulations, support and extend Lande's claim that drift along a line of equilibria can rapidly lead to sexual isolation and speciation. Furthermore, we show that rapid speciation can occur by drift in populations of appreciable size ( N_e ≥ 1000). These results are in sharp contrast to the opinion of many researchers and textbook writers who have argued that drift does not play an important role in speciation. We argue that drift may be a powerful amplifier of speciation under a wide variety of modeling assumptions, even when selection acts directly on female mating preferences.