SEXUAL SELECTION,MULTIPLE MALE ORNAMENTS,AND AGE‐ AND CONDITION‐DEPENDENT SIGNALING IN THE COMMON YELLOWTHROAT

In many animals, sexual selection has resulted in complex signaling systems in which males advertise aspects of their phenotypic or genetic quality through elaborate ornamentation and display behaviors. Different ornaments might convey different information or be directed at different receivers, but they might also be redundant signals of quality that function reliably at different times (ages) or in different contexts. We explored sexual selection and age‐ and condition‐dependent signaling in the common yellowthroat (Geothlypis trichas), a sexually dichromatic warbler with two prominent plumage ornaments—a melanin‐based, black facial “mask” and carotenoid‐based, UV‐yellow “bib.” In a three‐year study, variance among males in the number of social (M_w) and extra‐pair (M_e) mates generated strong sexual selection on mask and bib attributes. Some traits (mask size, bib yellow brightness) were correlated with male age and did not experience selection beyond age‐related increases in M_w and M_e. Other traits showed age‐specific (bib size) or age‐reversed (ultraviolet brightness) patterns of selection that paralleled changes in the information‐content of each ornament. The components of male fitness generating selection in young versus old males were distinct, reflecting different sources of variation in male fertilization success. Age‐ and context‐dependent changes in the strength, direction, and target of selection may help explain the maintenance of multiple ornaments in this and other species.     

THE SIGNIFICANCE OF GENETIC EROSION IN THE PROCESS OF EXTINCTION. IV. INBREEDING LOAD AND HETEROSIS IN RELATION TO POPULATION SIZE IN THE MINT SALVIA PRATENSIS

If, because of genetic erosion, the level of homozygosity in small populations is high, additional selfing will result in small reductions of fitness. In addition, in small populations with a long inbreeding history selection may have purged the population of its genetic load. Therefore, a positive relationship between population size (or level of genetic variation) and level of additional inbreeding depression, here referred to as inbreeding load, may be expected. In a previous study on the rare and threatened perennial Salvia pratensis, a positive correlation between population size and level of allozyme variation has been demonstrated. In the present study, the inbreeding load in six populations of varying size and allozyme variation was investigated. In the greenhouse, significant inbreeding load in mean seed weight, proportion of germination, plant size, regenerative capacity, and survival was demonstrated. In a field experiment with the two largest and the two smallest populations, survival of selfed progeny was 16% to 63% lower than survival of outcrossed progeny. In addition, survival of outcrossed progeny was, with the exception of the largest population, lower (16% to 37%) than of hybrid progeny, resulting from crosses between populations. Effects on plant size were qualitatively similar to the effects on survival, but these effects were variable in time because of differential survival of larger individuals. In all populations the total inbreeding load, that is, the effects on size and survival multiplicated, increased in time. It was demonstrated that inbreeding load in different characters may be independent. At no time and for no character was inbreeding load or the heterosis effect correlated to the mean number of alleles per locus, indicating that allozyme variation is not representative for variation at fitness loci in these populations. Combined with results of previous investigations, these results suggest that the small populations are in an early phase of the genetic erosion process. In this phase, allozyme variation, which is supposed to be (nearly) neutral, has been affected by genetic erosion but the selectively nonneutral variation is only slightly affected. These results stress the need for detailed information about the inbreeding history of small populations. The relative performance of selfed progeny was lowest in all populations, in the greenhouse as well as in the field, and inbreeding depression could still influence the extinction probabilities of the small populations.     

THE SIGNIFICANCE OF GENETIC EROSION IN THE PROCESS OF EXTINCTION. IV. INBREEDING DEPRESSION AND HETEROSIS EFFECTS CAUSED BY SELFING AND OUTCROSSING IN SCABIOSA COLUMBARIA

The effects of self-fertilization, within-population crosses (WPC) and between-population crosses (BPC) on progeny fitness were investigated in the greenhouse for Scabiosa columbaria populations of varying size. Plants grown from field collected seeds were hand pollinated to produce selfed, WPC, and BPC progeny. The performance of these progenies was examined throughout the entire life cycle. The different pollination treatments did not significantly affect germination, seedling-to-adult survival, flowering percentage and the number of flower heads. But severe inbreeding depression was demonstrated for biomass production, root development, adult survival, and seed set. Additionally, multiplicative fitness functions were calculated to compare relative fitnesses for progeny. On average, WPC progeny showed a more than 4-fold, and BPC progeny an almost 10-fold, advantage over selfed progeny, indicating that S. columbaria is highly susceptible to inbreeding. No clear relationship was found between population size and level of inbreeding depression, suggesting that the genetic load has not yet been reduced substantially in the small populations. A significant positive correlation was found between plant dry weight and total fitness. In two out of six populations, the differences between the effects of the pollination treatments on dry weight increased significantly when seedlings were grown under competitive conditions. This result is interpreted as an enhancement of inbreeding depression under these conditions. It is argued that improvement of the genetic exchange between populations may lower the probability of population extinction.     

GENETIC ARCHITECTURE OF INBREEDING DEPRESSION AND THE MAINTENANCE OF GAMETOPHYTIC SELF‐INCOMPATIBILITY

Gametophytic self‐incompatibility (GSI) is a widespread genetic system, which enables hermaphroditic plants to avoid self‐fertilization and mating with close relatives. Inbreeding depression is thought to be the major force maintaining SI; however, inbreeding depression is a dynamical variable that depends in particular on the mating system. In this article we use multilocus, individual‐based simulations to examine the coevolution of SI and inbreeding depression within finite populations. We focus on the conditions for the maintenance of SI when self‐compatible (SC) mutants are introduced in the population by recurrent mutation, and compare simulation results with predictions from an analytical model treating inbreeding depression as a fixed parameter (thereby neglecting effects of purging within the SC subpopulation). In agreement with previous models, we observe that the maintenance of SI is associated with high inbreeding depression and is facilitated by high rates of self‐pollination. Purging of deleterious mutations by SC mutants has little effect on the spread of those mutants as long as most deleterious alleles have weak fitness effects: in this case, the genetic architecture of inbreeding depression has little effect on the maintenance of SI. By contrast, purging may greatly enhance the spread of SC mutants when deleterious alleles have strong fitness effects.     

EXAMINING THE RISK OF INBREEDING DEPRESSION IN A NATURALLY RARE CETACEAN,THE VAQUITA (PHOCOENA SINUS)1

Uncertainty about the magnitude of various risks facing endangered species can paralyze conservation action. The vaquita is a naturally rare porpoise that has declined to the low hundreds of individuals because of gillnet mortality over the past 57 years. No variability in mitochondrial DNA (mtDNA) was found in vaquitas (n= 43). Because reducing gillnet mortality will require strong conservation action, the question was raised whether vaquitas are doomed because of inbreeding depression and whether, therefore, mitigation efforts would be futile. We use simulations to investigate the “doom hypothesis” by first asking whether the current level of genetic variability results from the recent decline or from historical factors. If fixation was historical then deleterious alleles could have been selected out of vaquitas over thousands of years, reducing concerns about inbreeding depression. Simulations showed that fixation most likely resulted from historical rather than recent loss. Of 1,000 simulations done at plausible abundances and mutation rates, 247 (84.3%) fixed before and 46 (15.7%) fixed during the recent decline. Fixation correlates with historical abundance, making it more likely that because vaquitas are fixed, they are also a naturally rate species. However, because studies on purging deleterious alleles have not shown purging to be universally beneficial we also examine the doom hypothesis using data on the response to inbreeding of a wide variety of captive animals. Responses are so variable that the doom hypothesis cannot be affirmed. We further explore whether more data from vaquitas would lead to conclusive results and found that the data required, such as the adult survival rate, will be impossible to obtain. We conclude that because the doom hypothesis cannot be affirmed this risk factor should not delay conservation actions.     

SEXUAL SELECTION CAN INCREASE THE EFFECT OF RANDOM GENETIC DRIFT—A QUANTITATIVE GENETIC MODEL OF POLYMORPHISM IN OOPHAGA PUMILIO,THE STRAWBERRY POISON‐DART FROG

The variation in color pattern between populations of the poison‐dart frog Oophaga pumilio across the Bocas del Toro archipelago in Panama is suggested to be due to sexual selection, as two other nonsexually selecting Dendrobatid species found in the same habitat and range do not exhibit this variation. We theoretically test this assertion using a quantitative genetic sexual selection model incorporating aposematic coloration and random drift. We find that sexual selection could cause the observed variation via a novel process we call “coupled drift.” Within our model, for certain parameter values, sexual selection forces frog color to closely follow the evolution of female preference. Any between‐population variation in preference due to genetic drift is passed on to color. If female preference in O. pumilio is strongly affected by drift, whereas color in the nonsexually selecting Dendrobatid species is not, coupled drift will cause increased between‐population phenotypic variation. However, with different parameter values, coupled drift will result in between‐population variation in color being suppressed compared to its neutral value, or in little or no effect. We suggest that coupled drift is a novel theoretical process that could have a role linking sexual selection with speciation both in O. pumilio, and perhaps more generally.     

MASS SEXUAL REPRODUCTION IN THE TOXIGENIC DIATOMS PSEUDO‐NITZSCHIA AUSTRALIS AND P. PUNGENS (BACILLARIOPHYCEAE) ON THE WASHINGTON COAST,USA1

Sexual reproduction is documented for the first time in field populations of the pennate diatoms Pseudo‐nitzschia australis Freng. and P. pungens (Grunow ex Cleve) Hasle (var. cingulata Villac and hybrids between var. cingulata and var. pungens). A bloom dominated by these species began on June 26, 2006, along Kalaloch Beach, Washington, USA, coincident with a drop in the Si(OH)₄:NO₃ ratio to below two. Multimodal size distributions were detected for both species, and synchronous auxosporulation occurred within the smallest size class during a 3‐week window. Auxospores and initial cells created a new class of large cells, and cells in the intermediate size classes increased in abundance during auxosporulation. Mating cells of both species were attached to colonies of surf‐zone diatoms. Paired gametangia, gametes, zygotes, auxospores, and large initial cells were found. Auxosporulation began first for P. pungens (June 30), apparently once a critical, high cell concentration was reached, followed by P. australis (July 5), when the total Pseudo‐nitzschia cell concentration reached 929,000 cells · L^?1. Low frequencies of auxosporulation occurred throughout the bloom but increased 4‐fold for P. australis and 3‐fold for P. pungens when macronutrients were reduced to low levels on July 11. A 2‐year life cycle was estimated for P. australis and 3 years for P. pungens, both with annual auxosporulation. Domoic acid (DA) in razor clams reached a maximum of 38 μg DA · g^?1 on July 18. A significant relationship existed between the percent of cells within the new size range and DA concentrations in razor clams on the same beach.     

EXPERIMENTAL EVIDENCE FOR THE EVOLUTION OF INDIRECT GENETIC EFFECTS: CHANGES IN THE INTERACTION EFFECT COEFFICIENT,PSI (Ψ), DUE TO SEXUAL SELECTION

Indirect genetics effects (IGEs)—when the genotype of one individual affects the phenotypic expression of a trait in another—may alter evolutionary trajectories beyond that predicted by standard quantitative genetic theory as a consequence of genotypic evolution of the social environment. For IGEs to occur, the trait of interest must respond to one or more indicator traits in interacting conspecifics. In quantitative genetic models of IGEs, these responses (reaction norms) are termed interaction effect coefficients and are represented by the parameter psi (Ψ). The extent to which Ψ exhibits genetic variation within a population, and may therefore itself evolve, is unknown. Using an experimental evolution approach, we provide evidence for a genetic basis to the phenotypic response caused by IGEs on sexual display traits in Drosophila serrata. We show that evolution of the response is affected by sexual but not natural selection when flies adapt to a novel environment. Our results indicate a further mechanism by which IGEs can alter evolutionary trajectories—the evolution of interaction effects themselves.     

MICROSATELLITE MARKER DEVELOPMENT AND GENETIC VARIATION IN THE TOXIC MARINE DIATOM PSEUDO‐NITZSCHIA MULTISERIES (BACILLARIOPHYCEAE)1

The genetic structure of phytoplankton populations is largely unknown. In this study we developed nine polymorphic microsatellite markers for the domoic acid–producing marine diatom Pseudo‐nitzschia multiseries (Hasle) Hasle. We then used them in the genotyping of 25 physiologically diverse field isolates and six of their descendants: 22 field isolates originated from eastern Canadian waters, two from European waters, and one from Russian waters. The numbers of alleles per locus ranged from three to seven and the observed heterozygosities from 0.39 to 0.70. A substantial degree of genetic variation was observed within the field isolates, with 23 different genotypes detected. The Russian isolate was the most genetically distinct, although there was also evidence of genetic differentiation at a more local scale. Mating experiments demonstrated that alleles were inherited in a Mendelian manner. Pseudo‐nitzschia multiseries primer pairs were tested on DNA from four congeners: P. calliantha Lundholm, Moestrup et Hasle; P. fraudulenta (P. T. Cleve) Hasle; P. pungens (Grunow ex P. T. Cleve) Hasle; and P. seriata (P. T. Cleve) H. Peragallo. Cross‐reactivity was only observed in P. pungens. Our results are a first step in understanding the genetic variation present at the Pseudo‐nitzschia“species” level and in determining the true biogeographic extent of Pseudo‐nitzschia species.     

SEX LINKAGE,SEX‐SPECIFIC SELECTION,AND THE ROLE OF RECOMBINATION IN THE EVOLUTION OF SEXUALLY DIMORPHIC GENE EXPRESSION

Sex‐biased genes—genes that are differentially expressed within males and females—are nonrandomly distributed across animal genomes, with sex chromosomes and autosomes often carrying markedly different concentrations of male‐ and female‐biased genes. These linkage patterns are often gene‐ and lineage‐dependent, differing between functional genetic categories and between species. Although sex‐specific selection is often hypothesized to shape the evolution of sex‐linked and autosomal gene content, population genetics theory has yet to account for many of the gene‐ and lineage‐specific idiosyncrasies emerging from the empirical literature. With the goal of improving the connection between evolutionary theory and a rapidly growing body of genome‐wide empirical studies, we extend previous population genetics theory of sex‐specific selection by developing and analyzing a biologically informed model that incorporates sex linkage, pleiotropy, recombination, and epistasis, factors that are likely to vary between genes and between species. Our results demonstrate that sex‐specific selection and sex‐specific recombination rates can generate, and are compatible with, the gene‐ and species‐specific linkage patterns reported in the genomics literature. The theory suggests that sexual selection may strongly influence the architectures of animal genomes, as well as the chromosomal distribution of fixed substitutions underlying sexually dimorphic traits.     

EVOLUTION OF RESISTANCE TO A MULTIPLE‐HERBIVORE COMMUNITY: GENETIC CORRELATIONS,DIFFUSE COEVOLUTION,AND CONSTRAINTS ON THE PLANT'S RESPONSE TO SELECTION

Although plants are generally attacked by a community of several species of herbivores, relatively little is known about the strength of natural selection for resistance in multiple‐herbivore communities—particularly how the strength of selection differs among herbivores that feed on different plant organs or how strongly genetic correlations in resistance affect the evolutionary responses of the plant. Here, we report on a field study measuring natural selection for resistance in a diverse community of herbivores of Solanum carolinense. Using linear phenotypic‐selection analyses, we found that directional selection acted to increase resistance to seven species. Selection was strongest to increase resistance to fruit feeders, followed by flower feeders, then leaf feeders. Selection favored a decrease in resistance to a stem borer. Bootstrapping analyses showed that the plant population contained significant genetic variation for each of 14 measured resistance traits and significant covariances in one‐third of the pairwise combinations of resistance traits. These genetic covariances reduced the plant's overall predicted evolutionary response for resistance against the herbivore community by about 60%. Diffuse (co)evolution was widespread in this community, and the diffuse interactions had an overwhelmingly constraining (rather than facilitative) effect on the plant's evolution of resistance.     

EFFECT OF ELEVATED TEMPERATURE,DARKNESS, AND HYDROGEN PEROXIDE TREATMENT ON OXIDATIVE STRESS AND CELL DEATH IN THE BLOOM‐FORMING TOXIC CYANOBACTERIUM MICROCYSTIS AERUGINOSA1

This study assessed the implication of oxidative stress in the mortality of cells of Microcystis aeruginosa Kütz. Cultures grown at 25°C were exposed to 32°C, darkness, and hydrogen peroxide (0.5 mM) for 96 h. The cellular abundance, chl a concentration and content, maximum photochemical efficiency of PSII (F_v/F_m ratio), intracellular oxidative stress (determined with dihydrorhodamine 123 [DHR]), cell mortality (revealed by SYTOX‐labeling of DNA), and activation of caspase 3–like proteins were assessed every 24 h. The presence of DNA degradation in cells of M. aeruginosa was also assessed using a terminal deoxynucletidyl transferase‐mediated dUTP nick end labeling (TUNEL) assay at 96 h. Transferring cultures from 25°C to 32°C was generally beneficial to the cells. The cellular abundance and chl a concentration increased, and the mortality remained low (except for a transient burst at 72 h) as did the oxidative stress. In darkness, cells did not divide, and the F_v/F_m continuously decreased with time. The slow increase in intracellular oxidative stress coincided with the activation of caspase 3–like proteins and a 15% and 17% increase in mortality and TUNEL‐positive cells, respectively. Exposure to hydrogen peroxide had the most detrimental effect on cells as growth ceased and the F_v/F_m declined to near zero in less than 24 h. The 2‐fold increase in oxidative stress matched the activation of caspase 3–like proteins and a 40% and 37% increase in mortality and TUNEL‐positive cells, respectively. These results demonstrate the implication of oxidative stress in the stress response and mortality of M. aeruginosa.