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In the past decade, the academic community has increased considerably its activity concerning the teaching and learning of evolution. Despite such beneficial activity, the state of public understanding of evolution is considered woefully lacking by most researchers and educators. This lack of understanding affects evolution/science literacy, research, and academia in general. Not only does the general public lack an understanding of evolution but so does a considerable proportion of college graduates. However, it is not just evolutionary concepts that students do not retain. In general, college students retain little of what they supposedly have learned. Worse yet, it is not just students who have avoided science and math who fail to retain fundamental science concepts. Students who have had extensive secondary-level and college courses in science have similar deficits. We examine these issues and explore what distinguishes effective pedagogy from ineffective pedagogy in higher education in general and evolution education in particular. The fundamental problem of students' prior conceptions is considered and why prior conceptions often underpin students' misunderstanding of the evolutionary concepts being taught. These conceptions can often be discovered and addressed. We also attend to concerns about coverage of course content and the influence of religious beliefs, and provide helpful strategies to improve college-level teaching of evolution.
Balancing selection in the form of heterozygote advantage, frequency-dependent selection, or selection that varies in time and/or space, has been proposed to explain the high variation at major histocompatibility complex (MHC) genes. Here the effect of variation of the presence and absence of pathogens over time on genetic variation at multiallelic loci is examined. In the basic model, resistance to each pathogen is conferred by a given allele, and this allele is assumed to be dominant. Given that s is the selective disadvantage for homozygotes (and heterozygotes) without the resistance allele and the proportion of generations, which a pathogen is present, is e, fitnesses for homozygotes become (1 − s)(n−1)e and the fitnesses for heterozygotes become (1 − s)(n−2)e, where n is the number of alleles. In this situation, the conditions for a stable, multiallelic polymorphism are met even though there is no intrinsic heterozygote advantage. The distribution of allele frequencies and consequently heterozygosity are a function of the autocorrelation of the presence of the pathogen in subsequent generations. When there is a positive autocorrelation over generations, the observed heterozygosity is reduced. In addition, the effects of lower levels of selection and dominance and the influence of genetic drift were examined. These effects were compared to the observed heterozygosity for two MHC genes in several South American Indian samples. Overall, resistance conferred by specific alleles to temporally variable pathogens may contribute to the observed polymorphism at MHC genes and other similar host defense loci.
Morphometric studies often consider parts with internal left-right symmetry, for instance, the vertebrate skull. This type of symmetry is called object symmetry and is distinguished from matching symmetry, in which two separate structures exist as mirror images of each other, one on each body side. We explain a method for partitioning the total shape variation of landmark configurations with object symmetry into components of symmetric variation among individuals and asymmetry. This method is based on the Procrustes superimposition of the original and a reflected copy of each landmark configuration and is compatible with the two-factor ANOVA model customary in studies of fluctuating asymmetry. We show a fully multivariate framework for testing the effects in the two-factor model with MANOVA statistics, which also applies to shapes with matching symmetry. We apply the new methods in a small case study of pharyngeal jaws of the Neotropical cichlid fish Amphilophus citrinellus. The analysis revealed that the symmetric component of variation in the pharyngeal jaws is dominated by the contrast between two alternative trophic morphs in this species and that there is subtle but statistically significant directional asymmetry. Finally, we provide some general recommendations for morphometric studies of symmetric shapes.
Molecular evolution has been considered to be essentially a stochastic process, little influenced by the pace of phenotypic change. This assumption was challenged by a study that demonstrated an association between rates of morphological and molecular change estimated for “total-evidence” phylogenies, a finding that led some researchers to challenge molecular date estimates of major evolutionary radiations. Here we show that Omland's (1997) result is probably due to methodological bias, particularly phylogenetic nonindependence, rather than being indicative of an underlying evolutionary phenomenon. We apply three new methods specifically designed to overcome phylogenetic bias to 13 published phylogenetic datasets for vertebrate taxa, each of which includes both morphological characters and DNA sequence data. We find no evidence of an association between rates of molecular and morphological rates of change.
Phylogenetic analyses and molecular dating estimates based on chloroplast DNA sequences were used to establish the relationships of the southern and Southeast Asian Crypteroniaceae and elucidate their biogeographic history. Maximum parsimony and likelihood analyses of rbcL sequences suggested that Crypteroniaceae should be restricted to Crypteronia, Axinandra, and Dactylocladus and that Crypteroniaceae, so defined, are sister to a clade formed by three small African taxa (Oliniaceae, Penaeaceae, and Rhynchocalycaceae) and the monotypic Central and South American Alzateaceae. Three molecular dating approaches (maximum-likelihood under a molecular clock, Langley-Fitch, and penalized-likelihood) were used to infer the age of Crypteroniaceae using both paleobotanic and geologic calibrations. Comparisons among these three methods revealed significant lineage effects in rbcL sequences. Clock-independent dating estimates suggested that divergence of Crypteroniaceae from its African and South American relatives coincided with the breakup of Gondwana, and that India likely served as a “raft” transporting Crypteroniaceae to Asia, with later expansion to Southeast Asia. To our knowledge, Crypteroniaceae are the first plant group for which the out-of-India hypothesis is well corroborated by molecular-based estimates of divergence times.
Natural hybridization occurs throughout areas of sympatry for the North American milkweeds Asclepias exaltata and A. syriaca (Asclepiadaceae), even though the formation of F1 hybrid seed is a rare event. For introgressive hybridization to proceed, F1 and advanced hybrids must be released from reproductive barriers and successfully mate with one or both parental species. I investigated the mating system of natural hybrids between A. exaltata and A. syriaca in three populations in Shenandoah National Park, Virginia. Allozyme data and a maximum-likelihood procedure were used to estimate the frequency of six genotypic classes (parentals, F1, F2, and backcrosses) of the hybridizing populations, the pollinia received by hybrid plants, and the paternal parents of seeds produced by hybrids. F1 hybrids, backcross A. syriaca, and parental A. syriaca individuals were common in three hybrid populations. Even though self-pollinations and interhybrid pollinations were common, F2 seed production and the occurrence of F2 individuals were rare in hybrid populations. Hybrid plants received more pollen from A. syriaca than A. exaltata, which resulted in the production of more backcross–A. syriaca seed than backcross–A. exaltata seed. Asclepias exaltata was rare in the hybrid populations, but A. exaltata pollinia were received by hybrids and this species sired between 15% and 36% of the seeds produced on hybrids. The potential for introgression with A. exaltata populations is lower because this species is unsuccessful as the maternal parent in interspecific and backcross hand-pollinations. The asymetry of hybridization with A. syriaca as the maternal parent is further supported by the incorporation of maternally inherited chloroplast DNA markers in hybrids. Hybrid milkweeds frequently backcross with both parental species and may be released from the reproductive barriers that limit the formation of F1 hybrids in natural populations. The direction of interspecific gene flow and introgression in milkweeds is influenced by the reproductive biology of hybrids, the constituency of the surrounding population, and failure of some crosses to produce seeds. Finally, introgressive hybridization remains an important evolutionary force even when the initial formation of F1 hybrids in natural populations is rare.
Direct development in benthic marine invertebrates is usually associated with narrow geographical range, low rates of colonization, and low levels of gene flow. Paradoxically, the small brittle star Amphipholis squamata broods its larvae to a crawl-away juvenile stage, yet has a cosmopolitan distribution. Using sequence and restriction-fragment-length-polymorphisms (RFLP) analyses of nuclear and mitochondrial DNA from 16 coastal populations throughout New Zealand, we tested whether the species is indeed a poor disperser, as may be expected from its brooding habit. We predicted that local and regional populations would be genetically structured according to isolation by distance. We also suspected that this ubiquitous “species” is composed of a variety of cryptic taxa in different geographic areas, as has been discovered in an increasing number of marine invertebrates. We found evidence of four genetically divergent and reproductively isolated lineages that can exist in syntopy. Lineages vary in abundance, haplotype diversity, and geographic distribution. The partitioning of genetic variation within the most common lineage, as well as the geographic distribution of the four lineages, suggest a north/south split. This pattern is consistent with known New Zealand marine biogeographic zones and appears to be linked to the regime of oceanic circulation, which is characterized by subtropical, southward-moving water masses in the north, and sub-Antarctic, northward-moving water in the south. We conclude that the dispersal ability of A. squamata is regionally restricted but with sporadic long-distance dispersal, which serves to increase local genetic variation. Our results support the idea that dispersal occurs through passive transport by drifting or rafting on macroalgae, which A. squamata commonly inhabits, and emphasize that poor dispersal ability is not necessarily a corollary of direct development.
Genetic variance, phenotypic variance, and the genetic covariance matrix (G) can change as a result of genetic drift. These changes will persist over time to some extent and will continue if population size remains relatively small. Nine populations founded by a single pair of Drosophila melanogaster were measured for a series of six morphological characteristics for a large number of parent-offspring families at both the third generation after the bottlenecks and after 20 generations. From these data, the phenotypic variance, additive genetic variance, and G were estimated for each line at each generation. Phenotypic and genetic variances were highly correlated over time, so that the measurements made at the third generation were predictive of the state of the population 17 generations later. Genetic covariances were also somewhat stable over time; however, the G matrices of some lines changed significantly over the intervening generations. This change did not return the populations toward their original state before the population bottlenecks. We conclude that the genetic covariance matrix can change as a result of mild genetic drift over a short span of time.
We have recently described a mutualistic symbiosis in which Wolbachia bacteria were shown to improve the fitness of some Drosophila melanogaster stocks. Wolbachia did not extend longevity in all Drosophila genotypes, even though 16s rDNA sequences indicated that our Drosophila stocks were infected with the same Wolbachia strain. Here, we use reciprocal hybrid crosses between two Drosophila strains, one that lived longer with Wolbachia (Z53) and one that did not (Z2), to investigate the inheritance of the survival phenotype and its dependence on the host genotype, sex, and mating conditions. Wolbachia's positive effects were more apparent in hybrid flies than in parental flies, ruling out exclusive maternal inheritance or the dependence of the survival phenotype on Wolbachia strain differences. The Wolbachia survival effects were more apparent in single-sex cages, where courtship and mating were not permitted. In these cages, nearly all flies with Wolbachia lived longer than uninfected flies, even though strain Z2 showed no Wolbachia effect in mixed-sex mating cages. We used comparisons between single- and mixed-sex cages to estimate the cost of reproduction for both sexes. Our data suggest that Wolbachia infection may increase the inferred cost of reproduction, particularly in males. Wolbachia can even produce a positive survival effect almost as large as the negative survival effect associated with reproduction. We discuss the implications of our experiments for the study of insect symbioses.
Aging appears to cease at late ages, when mortality rates roughly plateau in large-scale demographic studies. This anomalous plateau in late-life mortality has been explained theoretically in two ways: (1) as a strictly demographic result of heterogeneity in life-long robustness between individuals within cohorts, and (2) as an evolutionary result of the plateau in the force of natural selection after the end of reproduction. Here we test the latter theory using cohorts of Drosophila melanogaster cultured with different ages of reproduction for many generations. We show in two independent comparisons that populations that evolve with early truncation of reproduction exhibit earlier onset of mortality-rate plateaus, in conformity with evolutionary theory. In addition, we test two population genetic mechanisms that may be involved in the evolution of late-life mortality: mutation accumulation and antagonistic pleiotropy. We test mutation accumulation by crossing genetically divergent, yet demographically identical, populations, testing for hybrid vigor between the hybrid and nonhybrid parental populations. We found no difference between the hybrid and nonhybrid populations in late-life mortality rates, a result that does not support mutation accumulation as a genetic mechanism for late-life mortality, assuming mutations act recessively. Finally, we test antagonistic pleiotropy by returning replicate populations to a much earlier age of last reproduction for a short evolutionary time, testing for a rapid indirect response of late-life mortality rates. The positive results from this test support antagonistic pleiotropy as a genetic mechanism for the evolution of late-life mortality. Together these experiments comprise the first corroborations of the evolutionary theory of late-life mortality.
It has been proposed that a moving hybrid zone can be a mechanism for the spread of adaptive traits in phase III of Wright's shifting balance model of evolution. Here I present an example of a moving hybrid zone in warningly colored Heliconius butterflies, a system which is considered to be a possible case of shifting balance evolution. Having moved approximately 47 km in 17 years, the hybrid zone shift has led to the H. erato hydara color pattern rapidly displacing the adjacent H. erato petiverana pattern. The movement is potentially due to dominance drive augmenting a slight selective advantage of H. erato hydara over H. erato petiverana, which is largely consistent with theoretical conditions favoring the success of phase III.
Females, by mating with more than one male in their lifetime, may reduce their risk of receiving sperm from genetically incompatible sires or increase their prospects of obtaining sperm from genetically superior sires. Although there is evidence of both kinds of genetic benefits in crickets, their relative importance remains unclear, and the extent to which experimentally manipulated levels of polyandry in the laboratory correspond to those that occur in nature remain unknown. We measured lifetime polyandry of free-living female decorated crickets, Gryllodes sigillatus, and conducted an experiment to determine whether polyandry leads to an increase in offspring viability. We experimentally manipulated both the levels of polyandry and opportunities for females to select among males, randomly allocating the offspring of experimental females to high-food-stress or low-food-stress regimes to complete their development. Females exhibited a high degree of polyandry, mating on average with more than seven different males during their lifetime and up to as many as 15. Polyandry had no effect on either the developmental time or survival of offspring. However, polyandrous females produced significantly heavier sons than those of monandrous females, although there was no difference in the adult mass of daughters. There was no significant interaction between mating treatment and offspring nutritional regimen in their effects on offspring mass, suggesting that benefits accruing to female polyandry are independent of the environment in which offspring develop. The sex difference in the extent to which male and female offspring benefit via their mother's polyandry may reflect possible differences in the fitness returns from sons and daughters. The larger mass gain shown by sons of polyandrous females probably leads to their increased reproductive success, either because of their increased success in sperm competition or because of their increased life span.
In many polygynous social insect societies, ecological factors such as habitat saturation promote high queen numbers by increasing the cost of solitary breeding. If polygyny is associated with constrained environments, queen number in colonies of invasive social insects should increase as saturation of their new habitat increases. Here I describe the variation in queen number, nestmate relatedness, and nest size along a gradient of time since colonization in an invading population of Argentine ants (Linepithema humile) in Haleakala, Hawaii. Nest densities in this population increase with distance from the leading edge of the invasion, reaching a stable density plateau approximately 80 m from the edge (> 2 years after colonization). Although the number of queens per nest in Haleakala is generally lower than previously reported for Argentine ants, there is significant variation in queen number across this population. Both the observed and effective queen numbers increase across the density gradient, and nests in the center of the population contain queen numbers three to nine times higher than those on the edge of the invasion. The number of workers per nest is correlated with queen number, and nests in the center are six times larger than nests at the edge. Microsatellite analysis of relatedness among nestmates reveals that all nests in the Haleakala population are characterized by low relatedness and have evidence of multiple reproducing queens. Relatedness values are significantly lower in nests in the center of the population, indicating that the number of reproducing queens is greater in areas of high nest density. The variation in queen number and nestmate relatedness in this study is consistent with expectations based on changes in ecological constraints during the invasion of a new habitat, suggesting that the social structure of Argentine ant populations is strongly influenced by ecological factors. Flexibility in social structure may facilitate persistence in variable environments and may also confer significant advantages to a species when introduced into new areas.
Speciation of two social parasites from their respective hosts is tested using a molecular phylogeny. Alignment of 711 DNA base pairs of mitochondrial cytochrome b gene was used to assess phylogenetic relationships of inquiline species to their hosts and to other members of the genus. We show that the inquiline social parasites of the North American seed harvester ants are monophyletic, descending from one of the known hosts (Pogonomyrmex barbatus) in the recent past and shifting hosts in a pattern similar to that observed in other Hymenopteran social parasites. In addition, the host populations unexpectedly were found to be polyphyletic. Populations of Pogonomyrmex rugosus from an area east of the Chiricahua Mountains in Southern Arizona belong to a mitochondrial clade separate from the more western clade of P. rugosus from the Sonoran and Chihuahuan Deserts. Evidence of mitochondrial DNA introgression between P. rugosus and P. barbatus was also observed. We conclude that Emery's rule does not strictly hold for this system, but that the hosts and parasites are very closely related, supporting a loose definition of Emery's rule.
Larvae of the salamander Hynobius retardatus have two distinct morphs: normal and broad-headed, cannibal morphs. We performed three experiments to differentiate among the following hypotheses: The broad-headed morph is induced to allow: (1) feeding on nutritious conspecifics; (2) exclusion of strong competitors for food or space; or (3) feeding on large, tough prey when smaller prey items are unavailable. When newly hatched larvae were reared with a heterospecific, Rana pirica (an anuran amphibian) tadpoles, the broad-headed morph was induced more frequently compared with those reared with conspecifics. The phenotype expressed depended on the size of the tadpoles: The broad-headed morph occurred more frequently with small and the normal morph with large tadpoles. Metamorphosis occurred sooner in larvae fed conspecifics compared with those fed heterospecific tadpoles, and the mean growth rate of larvae fed conspecifics was significantly faster than that of those fed tadpoles, suggesting that the heterospecific tadpoles were less nutritive than the conspecifics. These results do not support the hypotheses that the broad-headed morph evolved for consuming conspecifics because of their better balance of nutrients or for excluding strong competitors for food or space. We tentatively conclude that the morph evolved to eat large, tough prey, including both conspecifics and heterospecific tadpoles. Because H. retardatus usually spawns very early in the spring in small ponds partially covered with ice and snow, newly hatched larvae may starve from the lack of proper food owing to extremely low water temperatures. Thus, the broad-headed morph of H. retardatus may represent a cold-habitat adaptation to overcome the severe circumstance when the only food items available are relatively large conspecifics or heterospecific tadpoles.
Geographic variation in selection pressures may result in population divergence and speciation, especially if sexual selection varies among populations. Yet spatial variation in targets and intensity of sexual selection is well studied in only a few species. Even more rare are simultaneous studies of multiple populations combining observations from natural settings with controlled behavioral experiments. We investigated how sexual selection varies among populations of the chuckwalla, Sauromalus obesus. Chuckwallas are sexually dimorphic in color, and males vary in coloration among populations. Using field observations and multiple regression techniques, we investigated how sexual selection acts on various male traits in three populations in which males differed in coloration. The influence of sexual selection on male coloration was then investigated in more detail using controlled experiments. Results from field observations indicate that phenotypic selection was acting on territory quality in all three populations. In two populations, selection was also acting either directly or indirectly on male coloration. Male color likely functions as an indicator of food resources to females because male color is based partly on carotenoid pigments. In controlled experiments, significantly more females from these two populations chose males with brighter colors over dull males, a result consistent with studies on carotenoid pigments in other taxa. In a third population, no evidence of sexual selection on male coloration was found in either the field study or controlled experiment. Lack of female preferences for male color in this population, in which chuckwalla densities are low and home ranges are large, may result from searching costs to females.
We examined the phylogeography and history of giant Galápagos tortoise populations based on mitochondrial DNA sequence data from 161 individuals from 21 sampling sites representing the 11 currently recognized extant taxa. Molecular clock and geological considerations indicate a founding of the monophyletic Galápagos lineage around 2–3 million years ago, which would allow for all the diversification to have occurred on extant islands. Founding events generally occurred from geologically older to younger islands with some islands colonized more than once. Six of the 11 named taxa can be associated with monophyletic maternal lineages. One, Geochelone porteri on Santa Cruz Island, consists of two distinct populations connected by the deepest node in the archipelago-wide phylogeny, whereas tortoises in northwest Santa Cruz are closely related to those on adjacent Pinzón Island. Volcan Wolf, the northernmost volcano of Isabela Island, consists of both a unique set of maternal lineages and recent migrants from other islands, indicating multiple colonizations possibly due to human transport or multiple colonization and partial elimination through competition. These genetic findings are consistent with the mixed morphology of tortoises on this volcano. No clear genetic differentiation between two taxa on the two southernmost volcanoes of Isabela was evident. Extinction of crucial populations by human activities confounds whether domed versus saddleback carapaces of different populations are mono- or polyphyletic. Our findings revealed a complex phylogeography and history for this tortoise radiation within an insular environment and have implications for efforts to conserve these endangered biological treasures.
The “geographic mosaic” approach to understanding coevolution is predicated on the existence of variable selection across the landscape of an interaction between species. A range of ecological factors, from differences in resource availability to differences in community composition, can generate such a mosaic of selection among populations, and thereby differences in the strength of coevolution. The result is a mixture of hotspots, where reciprocal selection is strong, and coldspots, where reciprocal selection is weak or absent, throughout the ranges of species. Population subdivision further provides the opportunity for nonadaptive forces, including gene flow, drift, and metapopulation dynamics, to influence the coevolutionary interaction between species. Some predicted results of this geographic mosaic of coevolution include maladapted or mismatched phenotypes, maintenance of high levels of polymorphism, and prevention of stable equilibrium trait combinations.
To evaluate the potential for the geographic mosaic to influence predator-prey coevolution, we investigated the geographic pattern of genetically determined TTX resistance in the garter snake Thamnophis sirtalis over much of the range of its ecological interaction with toxic newts of genus Taricha. We assayed TTX resistance in over 2900 garter snakes representing 333 families from 40 populations throughout western North America. Our results provide dramatic evidence that geographic structure is an important component in coevolutionary interactions between predators and prey. Resistance levels vary substantially (over three orders of magnitude) among populations and over short distances. The spatial array of variation is consistent with two areas of intense evolutionary response by predators (“hotspots”) surrounded by clines of decreasing resistance. Some general predictions of the geographic mosaic process are supported, including clinal variation in phenotypes, polymorphism in some populations, and divergent outcomes of the interaction between predator and prey. Conversely, our data provide little support for one of the major predictions, mismatched values of interacting traits. Two lines of evidence suggest selection is paramount in determining population variation in resistance. First, phylogenetic information indicates that two hotspots of TTX resistance have evolved independently. Second, in the one region that TTX levels in prey have been quantified, resistance and toxicity levels match almost perfectly over a wide phenotypic and geographic range. However, these results do not preclude the role the nonadaptive forces in generating the overall geographic mosaic of TTX resistance. Much work remains to fill in the geographic pattern of variation among prey populations and, just as importantly, to explore the variation in the ecology of the interaction that occurs within populations.
We analyzed the rate at which postzygotic incompatibilities accumulate in birds. Our purposes were to assess the role of intrinsic F1 hybrid infertility and inviability in the speciation process, and to compare rates of loss of fertility and viability between the sexes. Among our sample more than half the crosses between species in the same genus produce fertile hybrids. Complete loss of F1 hybrid fertility takes on the order of millions of years. Loss of F1 hybrid viability occurs over longer timescales than fertility: some viable hybrids have been produced between taxa that appear to have been separated for more than 55 my. There is strong support for Haldane's rule, with very few examples where the male has lower fitness than the female. However, in contrast to Drosophila, fertility of the homogametic sex in the F1 appears to be lost before viability of the heterogametic sex in the F1. We conclude that the time span of loss of intrinsic hybrid fertility and viability is often, but not always, longer than the time to speciation. Premating isolation is an important mechanism maintaining reproductive isolation in birds. In addition, other factors causing postzygotic reproductive isolation such as ecological causes of hybrid unfitness, reduced mating success of hybrids, and genetic incompatibilities in the F2s and backcrosses may often be involved in the speciation process.
Theory predicts that in small isolated populations random genetic drift can lead to phenotypic divergence; however this prediction has rarely been tested quantitatively in natural populations. Here we utilize natural repeated island colonization events by members of the avian species complex, Zosterops lateralis, to assess whether or not genetic drift alone is an adequate explanation for the observed patterns of microevolutionary divergence in morphology. Morphological and molecular genetic characteristics of island and mainland populations are compared to test three predictions of drift theory: (1) that the pattern of morphological change is idiosyncratic to each island; (2) that there is concordance between morphological and neutral genetic shifts across island populations; and (3) for populations whose time of colonization is known, that the rate of morphological change is sufficiently slow to be accounted for solely by genetic drift. Our results are not consistent with these predictions. First, the direction of size shifts was consistently towards larger size, suggesting the action of a nonrandom process. Second, patterns of morphological divergence among recently colonized populations showed little concordance with divergence in neutral genetic characters. Third, rate tests of morphological change showed that effective population sizes were not small enough for random processes alone to account for the magnitude of microevolutionary change. Altogether, these three lines of evidence suggest that drift alone is not an adequate explanation of morphological differentiation in recently colonized island Zosterops and therefore we suggest that the observed microevolutionary changes are largely a result of directional natural selection.
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