Pollen competition reduces inbreeding depression in Collinsia heterophylla (Plantaginaceae)

We tested two predictions of the hypothesis that competition between self-pollen may mitigate negative genetic effects of inbreeding in plants: (1) intense competition among self-pollen increases offspring fitness; and (2) pollen competition reduces the measured strength of inbreeding depression. We used Collinsia heterophylla (Plantaginaceae), an annual with a mixed mating system, to perform controlled crosses in which we varied both the size of the pollen load and the source of pollen (self vs. outcross). Fitness of selfed offspring was higher in the high pollen-load treatment. Our second prediction was also upheld: inbreeding depression was, on average, lower when large pollen loads were applied (11%) relative to the low pollen-load treatment (28%). The reduction was significant for two fitness components relatively late in the life-cycle: number of surviving seedlings and pollen-tube growth rate in vitro. These findings suggest that intermittent inbreeding, which leads to self-fertilization in plants with genetic loads, may select for traits that enhance pollen competition.     

Braincase evolution in suchian archosaurs (Reptilia: Diapsida): evidence from the rauisuchian Batrachotomus kupferzellensis

The osteology of an almost complete braincase of the rauisuchian archosaur Batrachotomus kupferzellensis Gower from the Middle Triassic of Germany is described. There is a possibly discrete epiotic ossification, the metotic fissure is undivided by bone (i.e. there is a metotic foramen), the medial wall of the otic capsule is mostly ossified, the cerebral branch of the internal carotid artery entered the lateral surface of the parabasisphenoid, the ventral ramus of the opisthotic is more prominent laterally than a strong subvertical ridge on the exoccipital and basioccipital that lies posterior to the external foramen for the hypoglossal nerve, and the perilymphatic foramen faces away from the otic capsule in a posterior direction. Braincase morphology in the rauisuchians Saurosuchus galilei , Postosuchus kirkpatricki, and Tikisuchus romeri is reviewed. A matrix of 27 braincase characters for 12 archosaurian taxa is analysed. The most parsimonious hypothesis is consistent with the currently orthodox view of archosaurian phylogeny, except in that aetosaurians are more closely related to crocodylomorphs than is any rauisuchian. This phylogeny is used in a brief interpretation of the evolution of derived braincase features present in extant crocodilians. © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society , 2002, 136 , 49–76.     

Effects of stress and phenotypic variation on inbreeding depression in Brassica rapa

Stressful environments are often said to increase the expression of inbreeding depression. Alternatively, Crow's "opportunity for selection" (the squared phenotypic coefficient of variation) sets a limit to how much selection can occur, constraining the magnitude of inbreeding depression. To test these hypotheses, we planted self- and cross-fertilized seeds of Brassica rapa into a factorial experiment that varied plant density and saline watering stresses. We then repeated the experiment, reducing the salt concentration. We observed considerable inbreeding depression, particularly for survival in the first experiment and growth in the second. Both stresses independently depressed plant performance. Families differed in their amounts of inbreeding depression and reaction norms across environments. Outcrossed progeny were sometimes more variable. Stresses had small and inconsistent effects on inbreeding depression and, when significant, tended to diminish it. Levels of phenotypic variability often predicted whether inbreeding depression would increase or decrease across environments and were particularly effective in predicting which traits display the most inbreeding depression. Thus, we find little support for the stress hypothesis and mixed support for the phenotypic variability hypothesis. Variable levels of phenotypic variation provide a parsimonious explanation for shifts in inbreeding depression that should be tested before invoking more complex hypotheses.     

Genetic load,inbreeding depression,and hybrid vigor covary with population size: An empirical evaluation of theoretical predictions

Reduced population size is thought to have strong consequences for evolutionary processes as it enhances the strength of genetic drift. In its interaction with selection, this is predicted to increase the genetic load, reduce inbreeding depression, and increase hybrid vigor, and in turn affect phenotypic evolution. Several of these predictions have been tested, but comprehensive studies controlling for confounding factors are scarce. Here, we show that populations of Daphnia magna, which vary strongly in genetic diversity, also differ in genetic load, inbreeding depression, and hybrid vigor in a way that strongly supports theoretical predictions. Inbreeding depression is positively correlated with genetic diversity (a proxy for N_e), and genetic load and hybrid vigor are negatively correlated with genetic diversity. These patterns remain significant after accounting for potential confounding factors and indicate that, in small populations, a large proportion of the segregation load is converted into fixed load. Overall, the results suggest that the nature of genetic variation for fitness‐related traits differs strongly between large and small populations. This has large consequences for evolutionary processes in natural populations, such as selection on dispersal, breeding systems, ageing, and local adaptation.     

Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating

Hermaphroditic individuals can produce both selfed and outcrossed progeny, termed mixed mating. General theory predicts that mixed-mating populations should evolve quickly toward high rates of selfing, driven by rapid purging of genetic load and loss of inbreeding depression (ID), but the substantial number of mixed-mating species observed in nature calls this prediction into question. Lower average ID reported for selfing than for outcrossing populations is consistent with purging and suggests that mixed-mating taxa in evolutionary transition will have intermediate ID. We compared the magnitude of ID from published estimates for highly selfing (r > 0.8), mixed-mating (0.2 ≤ r ≥ 0.8), and highly outcrossing (r < 0.2) plant populations across 58 species. We found that mixed-mating and outcrossing taxa have equally high average lifetime ID (δ= 0.58 and 0.54, respectively) and similar ID at each of four life-cycle stages. These results are not consistent with evolution toward selfing in most mixed-mating taxa. We suggest that prevention of purging by selective interference could explain stable mixed mating in many natural populations. We identify critical gaps in the empirical data on ID and outline key approaches to filling them.     

Variation of selfing rate and inbreeding depression among individuals and across generations within an admixed Cedrus population

We investigated the variation and short-term evolution of the selfing rate and inbreeding depression (ID) across three generations within a cedar forest that was established from admixture ca 1860. The mean selfing rate was 9.5%, ranging from 0 to 48% among 20 seed trees (estimated from paternally inherited chloroplast DNA). We computed the probability of selfing for each seed and we investigated ID by comparing selfed and outcrossed seeds within progenies, thus avoiding maternal effects. In all progenies, the germination rate was high (88–100%) and seedling mortality was low (0–12%). The germination dynamics differed significantly between selfed and outcrossed seeds within progenies in the founder gene pool but not in the following generations. This transient effect of selfing could be attributed to epistatic interactions in the original admixture. Regarding the seedling growth traits, the ID was low but significant: 8 and 6% for height and diameter growth, respectively. These rates did not vary among generations, suggesting minor gene effects. At this early stage, outcrossed seedlings outcompeted their selfed relatives, but not necessarily other selfed seedlings from other progenies. Thus, purging these slightly deleterious genes may only occur through within-family selection. Processes that maintain a high level of genetic diversity for fitness-related traits among progenies also reduce the efficiency of purging this part of the genetic load.     

High selfing and high inbreeding depression in peripheral populations of Juncus atratus

The mating system of a plant is the prime determinant of its population genetic structure. However, mating system effects may be modified by postzygotic mechanisms like inbreeding depression. Furthermore, historical as well as contemporary ecological factors and population characteristics, like the location within the species range can contribute to genetic variability. Using microsatellite markers we assessed the population genetic structure of the wind-pollinated Juncus atratus in 16 populations from peripheral and nearly central areas of the distribution range and studied the mating system of the species. In three peripheral populations, outcrossing rates at seeds stage were low (mean t(m) = 5.6%), suggesting a highly autogamous mating system. Despite this fact, on adult stage both individual heterozygosity (mean H(O) = 0.48) and gene diversity (mean H(E) = 0.58) were high even in small populations. Inbreeding coefficients were consistently low among all populations (mean F(IS) = 0.15). Within the three peripheral populations indirect estimates of lifetime inbreeding depression were surprisingly high (delta(eq) = 0.96) and inbreeding depression could be shown to act mostly on early seedling establishment. Similar conditions of autogamy combined with high inbreeding depression are typical for plants with a large lifetime genomic mutation rate that cannot avoid selfing by geitonogamy. However, the results presented here are unexpected for small-statured, herbaceous plants. Substantial genetic differentiation among all populations was found (mean F(ST) = 0.24). An isolation-by-distance pattern was apparent on large scale but not on local scale suggesting that the overall pattern was largely influenced by historical factors, e.g. colonization, whereas locally genetic drift was of greater importance than gene flow. Peripheral populations exhibited lower genetic diversity and higher inbreeding coefficients when compared with subcentral populations.     

Nuclear and chloroplast microsatellites reveal extreme population differentiation and limited gene flow in the Aegean endemic Brassica cretica (Brassicaceae)

Nuclear and chloroplast microsatellite markers were used to study population structure and gene flow among seven Cretan populations of the Aegean endemic plant species Brassica cretica (Brassicaceae). Both nuclear and chloroplast markers revealed exceptionally high levels of population differentiation (overall F(ST)=0.628 and 1.000, respectively) and relatively little within-population diversity (overall H(S)=0.211 and 0.000, respectively). Maximum-likelihood estimates of directional migration rates were low among all pairs of populations (average Nm=0.286). There was no evidence that differences in flower colour between populations had any influence on historical levels of gene flow. In addition, a haplotype network showed that all five chloroplast haplotypes found in the sample were closely related. Together, these results suggest that current patterns of diversification in B. cretica are mainly a result of genetic drift during the last half million years. The main conclusions from the present study are consistent with the prevailing hypothesis that plant diversification in the Aegean region is driven by random rather than adaptive differentiation among isolated populations.     

Granite outcrops as ancient islands in old landscapes: evidence from the phylogeography and population genetics of Eucalyptus caesia (Myrtaceae) in Western Australia

Granite outcrops represent an isolated island habitat and, in ancient landscapes, may harbour species with complex evolutionary histories. Phylogenetic analysis of these species may reveal the influences of evolutionary processes over long time frames. Phylogenetic relationships from chloroplast and nuclear genome analysis were investigated in Eucalyptus caesia , a bird-pollinated mallee endemic to granite outcrops in the South-western Australian Floristic Region. The results obtained revealed high population and haplotype divergence, suggesting restriction to the specific habitat of granite outcrops over long time frames with genetic drift as the most significant evolutionary force. The hypothesis of derivation of ssp. magna from ssp. caesia was not supported by the pattern of diversity in either the chloroplast or the nuclear genome and the two subspecies were not monophyletic. Eucalyptus caesia displays significant clonality yet little evidence of inbreeding depression, suggesting deleterious mutations causing inbreeding depression have been purged.  © 2008 Department of Environment and Conservation. Journal compilation © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 177–188.     

Resolving the conundrum of inbreeding depression but no inbreeding avoidance: Estimating sex‐specific selection on inbreeding by song sparrows (Melospiza melodia)

Inbreeding avoidance among interacting females and males is not always observed despite inbreeding depression in offspring fitness, creating an apparent “inbreeding paradox.” This paradox could be resolved if selection against inbreeding was in fact weak, despite inbreeding depression. However, the net magnitude and direction of selection on the degree to which females and males inbreed by pairing with relatives has not been explicitly estimated. We used long‐term pedigree data to estimate phenotypic selection gradients on the degree of inbreeding that female and male song sparrows (Melospiza melodia) expressed by forming socially persistent breeding pairs with relatives. Fitness was measured as the total numbers of offspring and grand offspring contributed to the population, and as corresponding expected numbers of identical‐by‐descent allele copies, thereby accounting for variation in offspring survival, reproduction, and relatedness associated with variation in parental inbreeding. Estimated selection gradients on the degree to which individuals paired with relatives were weakly positive in females, but negative in males that formed at least one socially persistent pairing. However, males that paired had higher mean fitness than males that remained socially unpaired. These analyses suggest that net selection against inbreeding may be weak in both sexes despite strong inbreeding depression, thereby resolving the “inbreeding paradox.”     

Fitness consequences of floral variation in Senecio jacobaea (Asteraceae): evidence from a segregating hybrid population and a resource manipulation experiment

The present study examines some of the ecological factors that might exert selection on floral morphology in Senecio jacobaea , a self-sterile composite which exhibits geographic variation in the frequency of rayed and discoid individuals. Regression analyses of phenotypic data from a large, segregating hybrid population, established in a semi-natural (garden) environment and studied over a 2-year period, revealed a negative relationship between the size of the rays and the average germination rate of the maternal seed crop, a pattern that can be attributed to the reduced germination speed of achenes from ray florets. There was no effect of ray size on the amount of cross-pollination achieved, the proportion of heads infested by larvae of seed flies ( Pegohylemyia ) and the amount of resources retained for the next flowering season. The lack of resource costs was also apparent in a manipulation experiment with greenhouse-grown plants of the rayed phenotype: artificial removal of all rays at the early bud or flowering stage had no detectable effect on subsequent flower and fruit development, regardless of whether the plants experienced high or low water stress. Given these and other observations, I hypothesize that plant-animal interactions and resource costs sometimes play a minor role in exerting selection on flower morphology and that spatially varying selection on germination behaviour accounts for some of the morph frequency variation in S. jacobaea.     

Floral reduction in Crepis tectorum (Asteraceae): tradeoffs and dominance relationships

The present investigation of Crepis tectorum examines the extent to which tradeoffs and patterns of dominance contribute to the association between flower size (head width) and degree of self-fertility among populations adapted to rock outcrops. Partial correlation analyses of phenotypic data from a F2 generation derived from a cross between two outcrop plants and of family means representing one of the parent populations indicate that small-flowered plants fail to reallocate resources to flower and fruit production, that small flower size offers little or no advantage in terms of autofertility, and that floral reduction has little influence on the rate of flower development. Hence, it may be necessary to invoke factors other than tradeoffs to explain the decline in flower size associated with the evolution of autogamy in C. tectorum. Comparison of parent and Fl hybrid means in the crossing experiment suggests incomplete dominance in the alleles for large flower size. Under the assumption that Fl hybrid means reflect the average degree of dominance across loci, I propose inbreeding depression as the basis for some of the reduction in floral morphology.     

The evolution of intrinsic reproductive isolation in the genus Cakile (Brassicaceae)

In theory, adaptive divergence can increase intrinsic post‐zygotic reproductive isolation (RI), either directly via selection on loci associated with RI, or indirectly via linkage of incompatibility loci with loci under selection. To test this hypothesis, we measured RI at five intrinsic post‐zygotic reproductive barriers between 18 taxa from the genera Cakile and Erucaria (Brassicaceae). Using a comparative framework, we tested whether the magnitude of RI was associated with genetic distance, geographic distance, ecological divergence and parental mating system. Early stages of post‐zygotic RI related to F₁ viability (i.e. initial seed set) tended to be stronger than later stages related to F₁ fecundity (i.e. flower number, fruit number). Mating system significantly influenced early stages of RI, such that RI was lowest when the mother was selfing and father was outcrossing, consistent with an imbalance between sink strength and resistance to provisioning. We found little evidence that adaptive divergence accelerates the evolution of intrinsic post‐zygotic RI, consistent with a nonecological model of evolution that predicts the nonlinear accumulation of RI and RI asymmetry with time (i.e. genetic distance), irrespective of adaptive divergence. Thus, although certain aspects of ecological divergence do not appear to have contributed strongly to the evolution of RI in this system, divergence in mating system actually reduced RI, suggesting that mating system evolution may play a significant role in speciation dynamics.     

Levels of inbreeding depression over seven generations of selfing in the androdioecious clam shrimp, Eulimnadia texana

Androdioecy (mixtures of males and hermaphrodites) is a rare mating system in both plants and animals. Theory suggests that high levels of inbreeding depression can maintain males in androdioecious populations if hermaphrodites commonly self-fertilize. However, if inbreeding depression (delta) can be 'purged' from selfing populations, maintaining males is more difficult. In the androdioecious clam shrimp, Eulimnadia texana, delta is estimated to be as high as 0.7. Previous work suggests that this high level is maintained in the face of high levels of inbreeding due to an associative overdominance of fitness-related loci with the sex-determining locus. Such associative overdominance would make purging of inbreeding depression difficult to impossible. The current experiment was designed to determine if delta can be purged in these shrimp by tracking fitness across seven generations in selfing and outcrossing treatments. Evidence of purging was found in one of four populations, but the remaining populations demonstrated a consistent pattern of delta across generations. Although the experimental design allowed ample opportunity for purging, the majority of populations were unable to purge their genetic load. Therefore, delta in this species is likely due to associative overdominance caused by deleterious recessive alleles linked to the sex determining locus.     

Accounting for cryptic population substructure enhances detection of inbreeding depression with genomic inbreeding coefficients: an example from a critically endangered marsupial

Characterizing inbreeding depression in wildlife populations can be critical to their conservation. Coefficients of individual inbreeding can be estimated from genome‐wide marker data. The degree to which sensitivity of inbreeding coefficients to population genetic substructure alters estimates of inbreeding depression in wild populations is not well understood. Using generalized linear models, we tested the power of two frequently used inbreeding coefficients that are calculated from genome‐wide SNP markers, F_H and F^^III, to predict four fitness traits estimated over two decades in an isolated population of the critically endangered Leadbeater's possum. F_H estimates inbreeding as excess observed homozygotes relative to equilibrium expectations, whereas F^^III quantifies allelic similarity between the gametes that formed an individual, and upweights rare homozygotes. We estimated F_H and F^^III from 1,575 genome‐wide SNP loci in individuals with fitness trait data (N = 179–237 per trait), and computed revised coefficients, F_H^{by group} and F^^{IIIby group}, adjusted for population genetic substructure by calculating them separately within two different genetic groups of individuals identified in the population. Using F_H or F^^III in the models, inbreeding depression was detected for survival to sexual maturity, longevity and whether individuals bred during their lifetime. F^^{IIIby group} (but not F_H^{by group}) additionally revealed significant inbreeding depression for lifetime reproductive output (total offspring assigned to each individual). Estimates of numbers of lethal equivalents indicated substantial inbreeding load, but differing between inbreeding estimators. Inbreeding depression, declining population size, and low and declining genetic diversity suggest that genetic rescue may assist in preventing extinction of this unique Leadbeater's possum population.     

Reduced inbreeding depression in peripheral relative to central populations of a monocarpic herb

Many temperate taxa were confined to warmer latitudes during the last glacial maximum. As their ranges expanded when climates warmed, genetic drift and inbreeding in relatively small peripheral populations are expected to have reduced genetic diversity and the segregating genetic load. Therefore, inbreeding depression in peripheral populations might be lower than in centrally located sites. We evaluated the consequences of inbreeding for fitness traits in six central and six northern peripheral populations of the herb Campanulastrum americanum. Inbreeding reduced performance for all traits. Inbreeding depression in peripheral populations was lower than in central populations. This difference increased across the life cycle from similar levels for germination, to central populations having three times the inbreeding depression for adult traits. Geographical patterns of inbreeding depression suggest that mating system variation and potential future mating system evolution in many temperate taxa might reflect, at least in part, nonequilibrium conditions associated with historic range changes.     

Phenotypic selection in a natural population of Impatiens pallida Nutt. (Balsaminaceae)

In the annual plant Impatiens pallida, individuals exhibit a floral heteromorphism consisting of autogamously selfing, cleistogamous (CL) flowers and partially outcrossing, chasmogamous (CH) flowers. As part of an investigation into natural selection and mating system evolution in I. pallida, we measured the magnitude and direction of phenotypic selection on nine life history characters (two traits measured on three dates, one measured on two dates and one measured once). Three of these characters were positively correlated with the ratio of CH/CL flowers produced per plant, which is an important determinant of the mating system. Values for the nine characters and three different measures of fitness (viability, fecundity, lifetime) were estimated for 500 plants in five locations over a single growing season. Based on lifetime fitness, linear selection differentials were significant for all nine characters, indicating a selective advantage to tall, leafy, highly branched plants that flowered early. However, only two of these characters had a direct effect on fitness. Selection was significant on all nine characters when based on fecundity as well as lifetime fitness; however, only three of five characters examined had significant selection based on viability fitness. For all fitness components, the frequency of significant linear and nonlinear selection coefficients was comparable (23% vs 17% of all cases, respectively), but nonlinear coefficients were generally larger. Finally, the magnitude and direction of direct linear selection was heterogeneous among locations, for all characters and all fitness components. Collectively these results suggest that selection is strong, favouring large size, high allocation to reproduction and high CH/CL flower ratios. However, any directional evolutionary changes in vegetative or reproductive characters may be constrained by strong non-linear and correlational selection.     

Inbreeding depression is high in a self‐incompatible perennial herb population but absent in a self‐compatible population showing mixed mating

High inbreeding depression is thought to be one of the major factors preventing evolutionary transitions in hermaphroditic plants from self‐incompatibility (SI) and outcrossing toward self‐compatibility (SC) and selfing. However, when selfing does evolve, inbreeding depression can be quickly purged, allowing the evolution of complete self‐fertilization. In contrast, populations that show intermediate selfing rates (a mixed‐mating system) typically show levels of inbreeding depression similar to those in outcrossing species, suggesting that selection against inbreeding might be responsible for preventing the transition toward complete self‐fertilization. By implication, crosses among populations should reveal patterns of heterosis for mixed‐mating populations that are similar to those expected for outcrossing populations. Using hand‐pollination crosses, we compared levels of inbreeding depression and heterosis between populations of Linaria cavanillesii (Plantaginaceae), a perennial herb showing contrasting mating systems. The SI population showed high inbreeding depression, whereas the SC population displaying mixed mating showed no inbreeding depression. In contrast, we found that heterosis based on between‐population crosses was similar for SI and SC populations. Our results are consistent with the rapid purging of inbreeding depression in the derived SC population, despite the persistence of mixed mating. However, the maintenance of outcrossing after a transition to SC is inconsistent with the prediction that populations that have purged their inbreeding depression should evolve toward complete selfing, suggesting that the transition to SC in L. cavanillesii has been recent. SC in L. cavanillesii thus exemplifies a situation in which the mating system is likely not at an equilibrium with inbreeding depression.     

Impact of selective logging on inbreeding and gene dispersal in an Amazonian tree population of Carapa guianensis Aubl

Selective logging may impact patterns of genetic diversity within populations of harvested forest tree species by increasing distances separating conspecific trees, and modifying physical and biotic features of the forest habitat. We measured levels of gene diversity, inbreeding, pollen dispersal and spatial genetic structure (SGS) of an Amazonian insect-pollinated Carapa guianensis population before and after commercial selective logging. Similar levels of gene diversity and allelic richness were found before and after logging in both the adult and the seed generations. Pre- and post-harvest outcrossing rates were high, and not significantly different from one another. We found no significant levels of biparental inbreeding either before or after logging. Low levels of pollen pool differentiation were found, and the pre- vs. post-harvest difference was not significant. Pollen dispersal distance estimates averaged between 75 m and 265 m before logging, and between 76 m and 268 m after logging, depending on the value of tree density and the dispersal model used. There were weak and similar levels of differentiation of allele frequencies in the adults and in the pollen pool, before and after logging occurred, as well as weak and similar pre- and post-harvest levels of SGS among adult trees. The large neighbourhood sizes estimated suggest high historical levels of gene flow. Overall our results indicate that there is no clear short-term genetic impact of selective logging on this population of C. guianensis.