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Whole-genome characterization of embryonic stage inbreeding depression in a selfed loblolly pine family.

Inbreeding depression is important in the evolution of plant populations and mating systems. Previous studies have suggested that early-acting inbreeding depression in plants is primarily due to lethal alleles and possibly epistatic interactions. Recent advances in molecular markers now make genetic mapping a powerful tool to study the genetic architecture of inbreeding depression. We describe a genome-wide evaluation of embryonic viability loci in a selfed family of loblolly pine (Pinus taeda L.), using data from AFLP markers from an essentially complete genome map. Locus positions and effects were estimated from segregation ratios using a maximum-likelihood interval mapping procedure. We identified 19 loci showing moderately deleterious to lethal embryonic effects. These loci account for >13 lethal equivalents, greater than the average of 8.5 lethal equivalents reported for loblolly pine. Viability alleles show predominantly recessive action, although potential overdominance occurs at 3 loci. We found no evidence for epistasis in the distribution of pairwise marker correlations or in the regression of fitness on the number of markers linked to deleterious alleles. The predominant role of semilethal alleles in embryonic inbreeding depression has implications for the evolution of isolated populations and for genetic conservation and breeding programs in conifers.

Crosses, Genetic↗

An inbreeding model of associative overdominance during a population bottleneck.

Associative overdominance, the fitness difference between heterozygotes and homozygotes at a neutral locus, is classically described using two categories of models: linkage disequilibrium in small populations or identity disequilibrium in infinite, partially selfing populations. In both cases, only equilibrium situations have been considered. In the present study, associative overdominance is related to the distribution of individual inbreeding levels (i.e., genomic autozygosity). Our model integrates the effects of physical linkage and variation in inbreeding history among individual pedigrees. Hence, linkage and identity disequilibrium, traditionally presented as alternatives, are summarized within a single framework. This allows studying nonequilibrium situations in which both occur simultaneously. The model is applied to the case of an infinite population undergoing a sustained population bottleneck. The effects of bottleneck size, mating system, marker gene diversity, deleterious genomic mutation parameters, and physical linkage are evaluated. Bottlenecks transiently generate much larger associative overdominance than observed in equilibrium finite populations and represent a plausible explanation of empirical results obtained, for instance, in marine species. Moreover, the main origin of associative overdominance is random variation in individual inbreeding whereas physical linkage has little effect.

Animals↗

Population dynamics of an Ac-like transposable element in self- and cross-pollinating arabidopsis.

Theoretical models predict that the mating system should be an important factor driving the dynamics of transposable elements in natural populations due to differences in selective pressure on both element and host. We used a PCR-based approach to examine the abundance and levels of insertion polymorphism of Ac-III, a recently identified Ac-like transposon family, in natural populations of the selfing plant Arabidopsis thaliana and its close outcrossing relative, Arabidopsis lyrata. Although several insertions appeared to be ancient and shared between species, there is strong evidence for recent activity of this element family in both species. Sequences of the regions flanking insertions indicate that all Ac-III transposons segregating in natural populations are in noncoding regions and provide no evidence for local transposition events. Transposon display analysis suggests the presence of slightly higher numbers of insertion sites per individual but fewer total polymorphic insertions in the self-pollinating A. thaliana than A. lyrata. Element insertions appear to be segregating at significantly lower frequencies in A. lyrata than A. thaliana, which is consistent with a reduction in transposition rate, reduction in effective population size, or reduced efficacy of natural selection against element insertions in selfing populations.

Arabidopsis↗

Patterns of inbreeding depression and architecture of the load in subdivided populations.

Inbreeding depression is a general phenomenon that is due mainly to recessive deleterious mutations, the so-called mutation load. It has been much studied theoretically. However, until very recently, population structure has not been taken into account, even though it can be an important factor in the evolution of populations. Population subdivision modifies the dynamics of deleterious mutations because the outcome of selection depends on processes both within populations (selection and drift) and between populations (migration). Here, we present a general model that permits us to gain insight into patterns of inbreeding depression, heterosis, and the load in subdivided populations. We show that they can be interpreted with reference to single-population theory, using an appropriate local effective population size that integrates the effects of drift, selection, and migration. We term this the "effective population size of selection" (NS(e)). For the infinite island model, for example, it is equal to NS(e) = N1 + m/hs, where N is the local population size, m the migration rate, and h and s the dominance and selection coefficients of deleterious mutation. Our results have implications for the estimation and interpretation of inbreeding depression in subdivided populations, especially regarding conservation issues. We also discuss the possible effects of migration and subdivision on the evolution of mating systems.

Animals↗

Genetic organization and adaptive response of allozymes to ecological variables in Fundulus heteroclitus.

Populations of Fundulus heteroclitus, (Cyprinodontidae) a widespread coastal marine fish, were studied in control and artificially heated environments on the North Shore of Long Island, New York to determine (1) patterns of variation in biochemical phenotypes and (2) the extent to which this variation reflected adaptation to environmental characteristics. Variation at three of twelve polymorphic isoenzyme loci from the warm water population was beyond the range of variation among control populations, and resembled those determined for populations living at more southern latitudes. Hence, these differences were interpreted as adaptations to warm environments. Significant differences in allele frequencies and zygotic proportions at ten of twelve isoenzyme loci were found associated with differences in environments, sexes, and/or age classes. These data strongly support the view that protein polymorphisms are adaptive. Several observations suggested that selection acts upon multilocus phenotypes rather than upon those of single loci. Several di-locus phenotypic distributions were demonstrated to be nonrandom, and those that exhibited similar patterns of dependence over years were postulated to be maintained by selection. Highly heterozygous fish exhibited superior viability when cohorts were compared over successive years. The consequences of the polygynous mating system in this species for maintaining genetic variation and for allowing rapid evolutionary response to a variable environment are discussed.

Alleles↗

Accuracy and precision of methods to estimate the number of parents contributing to a half-sib progeny array.

Molecular technologies have made feasible large-scale studies of genetic parentage in nature by permitting the genotypic examination of hundreds or thousands of progeny. One common goal of such studies is to estimate the true number of unshared parents who contributed to a large half-sib progeny array. Here we introduce computer programs designed to count the number of gametotypes contributed by unshared parents to each such progeny array, as well as assess the accuracy and precision of various estimators for the true number of unshared parents via computer simulation. These simulations indicate that under most biological conditions (1) a traditional approach (the multilocus MINIMUM METHOD) that merely counts the number of distinct haplotypes in offspring and divides by 2L, where L is the number of loci assayed, often vastly underestimates the true number of unshared parents who contributed to a half-sib progeny array; (2) a recently developed HAPLOTYPES estimator is a considerable improvement over the MINIMUM METHOD when parental numbers are high; and (3) the accuracy and precision of the HAPLOTYPES estimator increase as marker polymorphism and sample size increase, or as reproductive skew and the number of parents contributing to the progeny array decrease. Generally, HAPLOTYPES-based estimates of parental numbers in large half-sib cohorts should improve the characterization of organismal reproductive strategies and mating systems from genetic data.

Animals↗

Group-structured genetic models in analyses of the population and behavioral ecology of poikilothermic vertebrates.

Estimates of gene correlations among individuals within and among populations are frequently derived from statistical analyses of genetic data (e.g., F statistics). These measures can be important tools in molecular ecology and conservation, and offer important insights into population breeding structure. Using recently derived theory developed for group-structured populations, we show that fixation indices, when combined with basic population ecological and demographic data can be used to investigate population mating systems and to predict dispersal rates, trajectories and asymptotic levels of fixation indices, and effective population size. Four case studies of poikilothermic vertebrates are used to demonstrate the broad utility of evolutionary and ecological inferences afforded by group-structured models.

Animals↗

High levels of genetic polymorphism in the insular endemic herb Jepsonia malvifolia.

Jepsonia malvifolia is a long-lived perennial herb endemic to the Channel Islands of southern California and Guadalupe Island, Mexico. Twelve populations of J. malvifolia on San Clemente Island were surveyed for their genotype at 21 allozyme loci, revealing high levels of genetic polymorphism. For all individuals across San Clemente Island, 95.2% of loci are polymorphic with A(p) = 2.90 and H(e) = 0.179. Populations averaged 60.2% polymorphic loci with A(p) = 2.42 and H(e) = 0.158. Most variation is found within rather than among populations (G(ST) = 0.101), although differentiation among populations is significant. Genetic identities range from 0.936 to 0.999 with mean I = 0.975. There is no significant relationship between genetic and geographic distance. Gene flow among populations is Nm = 9.5 based on private alleles and Nm = 2.2 based on F(ST). Outcrossing rates based on fixation indices average t = 0.753, indicating a primarily outcrossed mating system. The genetic variation observed is unusually high for an insular endemic herb and indicates that J. malvifolia is unlikely to be endangered by genetic factors.

Enzymes↗

Fine-scale genetic structure and fire-created habitat patchiness in the Australian allodapine bee, Exoneura nigrescens (Hymenoptera: Apidae).

Fire promotes an abundance of nest sites for the stem nesting bee Exoneura nigrescens, which remain viable for approximately 10 years. The finite duration of nesting substrate and localized fire events suggest that migration should minimize genetic structure among suitable habitat patches. Exoneura nigrescens was sampled from 7 localities with a known fire history in southwestern Victoria, Australia. Individual bees were genotyped at 8 microsatellite loci and genic and genotypic analyses applied to examine genetic structure among burn patch localities, within burn patches, and within colonies. Despite relatively short-term availability of nesting substrates, remarkably fine-scale genetic structure was observed both among burn patches and within burn patches. The spatial distribution of relatedness shows a strong pattern of isolation-by-distance at geographic distances to 35 km, suggesting that genetic partitioning among burn patches is, at least in part, a result of dispersal ability. Genetic structure within burn patches includes colonies consisting of close kin with genic partitioning among nests. Relatedness structure within colonies suggests that polygamy, multiple breeding pairs, and a lack of inbreeding typifies the mating system.

Animals↗

Dietary alkaloids and the development of androconial organs in Estigmene acrea.

Male salt marsh moths, Estigmene acrea (Lepidoptera: Arctiidae), possess inflatable androconial organs called coremata. Prior to mating males form aggregations and inflate their coremata en masse. The communal display attracts additional males and females for the purpose of mating. The coremata are known to carry the plant-derived dihydropyrrolizine, hydroxydanaidal. This pheromonal substance is derived from secondary plant chemicals called pyrrolizidine alkaloids found in the larval diet. When E. acrea larvae were raised on semi-synthetic diets containing different levels of the pyrrolizidine alkaloid precursors the alkaloids triggered a pronounced morphogenetic effect. Adult males that fed on high levels of the pyrrolizidine alkaloid monocrotaline N-oxide (2500 microg) developed the largest coremata. Males that fed on lower levels of monocrotaline N-oxide (500 microg) or no alkaloid, while normal in body weight, had coremata that were progressively smaller and less robust. The size of the coremata and their commensurate pheromonal charge may have behavioral consequences in the unusual mating system of this species.

Animals↗

Evolution of the Sry genes.

Existing DNA sequence data on the Sry gene, the mammalian sex-determining locus in the Y chromosome, were analyzed for primates, rodents, and bovids. In all three taxonomic groups, the terminal sequences evolved faster than the HMG (high mobility group) boxes, and this applies both to synonymous (Ks) and nonsynonymous (Ka) nucleotide substitutions. Similar intragenic correlation between synonymous and nonsynonymous substitution rates was not found either in other mammalian genes that contain a conservative box (Sox, Msx) or in the MADS-box genes of plants. The rate of nonsynonymous substitutions exceeds significantly that of synonymous substitutions in the terminal Sry sequences of apes. We did not find good support for the hypothesis that the high evolutionary rate of Sry would be associated with a promiscuous mating system.

Animals↗

Contrasting patterns of nucleotide polymorphism at the alcohol dehydrogenase locus in the outcrossing Arabidopsis lyrata and the selfing Arabidopsis thaliana.

Nucleotide variation at the alcohol dehydrogenase locus (Adh) was studied in the outcrossing Arabidopsis lyrata, a close relative of the selfing Arabidopsis thaliana. Overall, estimated nucleotide diversity in the North American ssp. lyrata and two European ssp. petraea populations was 0.0038, lower than the corresponding specieswide estimate for A. thaliana at the same set of nucleotide sites. The distribution of segregating sites across the gene differed between the two species. Estimated sequence diversity within an A. lyrata population with a large sample size (0.0023) was much higher than has previously been observed for A. thaliana. This North American population has an excess of sites at intermediate frequencies compared with neutral expectation (Tajima's D = 2.3, P < 0.005), suggestive of linked balancing selection or a recent population bottleneck. In contrast, an excess of rare polymorphisms has been found in A. thaliana. Polymorphism within A. lyrata and divergence from A. thaliana appear to be correlated across the Adh gene sequence. The geographic distribution of polymorphism was quite different from that of A. thaliana, for which earlier studies of several genes found low within-population nucleotide site polymorphism and no overall continental differentiation of variation despite large differences in site frequencies between local populations. Differences between the outcrossing A. lyrata and the selfing A. thaliana reflect the impact of differences in mating system and the influence of bottlenecks in A. thaliana during rapid colonization on DNA sequence polymorphism. The influence of additional variability-reducing mechanisms, such as background selection or hitchhiking, may not be discernible.

Alcohol Dehydrogenase↗

Limited male incubation ability and the evolution of egg size in shorebirds.

In bird species where males incubate but are smaller than females, egg size may be constrained by male body size, and hence ability to incubate the eggs. Using data from 71 such shorebird species, we show that egg size decreases as the degree of female-biased sexual size dimorphism increases, after controlling for female body mass. Relative egg size was not related to mean clutch size. However, when controlling for mating system, the relationship between female-biased sexual size dimorphism and relative egg size was only significant in polyandrous species. The relatively small eggs of socially polyandrous shorebirds have previously been explained as an energy-saving strategy associated with the production of multiple clutches. Our findings suggest that egg size evolution is better explained by male incubation limitation in these birds.

Animals↗

A model of gender modification in gynodioecious plants.

The conditions under which hermaphrodites in gynodioecious populations might evolve increased allocation to male function are important for understanding the evolution of plant mating systems. A model is presented here that investigates these conditions under the assumptions that sex determination is nucleo-cytoplasmic and polymorphism is maintained by population subdivision. It is found that modifiers affecting the sex allocation in gynodioecious populations can invade under restrictive conditions, and that under these conditions hermaphroditism no longer is an evolutionary stable strategy. The reasons for the differences between this and related models are discussed.

Alleles↗

Outcrossing rates and correlated matings in a predominantly selfing freshwater snail.

We estimated outcrossing rates and correlated matings in a natural population of the hermaphroditic freshwater snail Ancylus fluviatilis, using progeny arrays and polymorphic allozyme markers. This design circumvents drawbacks of earlier studies, and yields maximum likelihood estimates of outcrossing rates at both the individual and population level. Adult snails were sampled during the spring breeding period, allowing for prior copulations and sperm transfer under natural conditions. Once in the laboratory, they were kept isolated for 21 days and laid egg capsules, and emerging hatchlings from 42 families were scored for five polymorphic loci. 87 of 848 offspring exhibited non-maternal alleles, representing a minimum population-level outcrossing of 10.3%. Maximum likelihood estimates are in the range 13-15%. Importantly, there is significant among-family heterogeneity, as only 16 of 42 families are estimated to have outcrossed, in accord with high estimates of correlated selfing within progeny arrays. Moreover, the high proportion of full sibs among outcrossed sibs suggests a limited extent of multiple paternity. Our data reveal important heterogeneity in the mating system of an animal hermaphrodite, and indicate the potential for evolutionary change in the breeding system.

Animals↗

Resolution of the phylogenetic position of the Congo peafowl, Afropavo congensis: a biogeographic and evolutionary enigma.

Afropavo congensis, the Congo peafowl, has long fascinated ornithologists because of its uncertain phylogenetic position and unusual geographic distribution. While some researchers have placed Afropavo as a sister taxon to the true peafowl, Pavo species, others have suggested relationships with the guineafowl or an Old World partridge, Francolinus. These divergent opinions are due, at least in part, to (i) the unique morphological characteristics, lack of elaborate ornamentation, and monogamous mating system in Afropavo which differentiates it from Pavo; and (ii) the restricted distribution of Afropavo in Zaire, which is far removed from the Asian distribution of all other pheasant species. We obtained complete cytochrome b and partial D-loop sequences of Afropavo and compared them to Pavo, guineafowl, Francolinus and other galliform taxa. Our results strongly support a close relationship between Afropavo and Pavo, and we were able to reject alternative phylogenetic hypotheses. Molecular clock estimates of the divergence time place the separation of Afropavo and Pavo in the late Miocene. We also discuss other relatives of Afropavo and Pavo and use this information to propose hypotheses regarding the evolution of ornamentation and sexual dimorphism within this group of pheasants.

Animals↗

Sexual reproduction and population dynamics: the role of polygyny and demographic sex differences.

Most models of population dynamics do not take sexual reproduction into account (i.e., they do not consider the role of males). However, assumptions behind this practice--that no demographic sex differences exist and males are always abundant enough to fertilize all the females--are usually not justified in natural populations. On the contrary, demographic sex differences are common, especially in polygynous species. Previous models that consider sexual reproduction report a stabilizing effect through mixing of different genotypes, thus suggesting a decrease in the propensity for complex of dynamics in sexually reproducing populations. Here we show that considering the direct role of males in reproduction and density dependence leads to the conclusion that a two-sex model is not necessarily more stable compared with the corresponding one-sex model. Although solutions exist where sexual reproduction has a stabilizing effect even when no genotypic variability is included (primarily when associated with monogamy), factors like polygyny, sex differences in survival or density dependence, and possible alterations of the primary sex ratio (the Trivers-Willard mechanism), may enlarge the parametric region of complex dynamics. Sexual reproduction therefore does not necessarily increase the stability of population dynamics and can have destabilizing effects, at least in species with complicated mating systems and sexual dimorphism.

Animals↗

Adaptive sex ratio variation in pre-industrial human (Homo sapiens) populations?

Sex allocation theory predicts that in a population with a biased operational sex ratio (OSR), parents will increase their fitness by adjusting the sex ratio of their progeny towards the rarer sex, until OSR has reached a level where the overproduction of either sex no longer increases a parent's probability of having grandchildren. Furthermore, in a monogamous mating system, a biased OSR is expected to lead to lowered mean fecundity among individuals of the more abundant sex. We studied the influence of OSR on the sex ratio of newborns and on the population birth rate using an extensive data set (n = 14,420 births) from pre-industrial (1775-1850) Finland. The overall effect of current OSR on sex ratio at birth was significant, and in the majority of the 21 parishes included in this study, more sons were produced when males were rarer than females. This suggests that humans adjusted the sex ratio of their offspring in response to the local OSR to maximize the reproductive success of their progeny. Birth rate and, presumably, also population growth rate increased when the sex ratio (males:females) among reproductive age classes approached equality. However, the strength of these patterns varied across the parishes, suggesting that factors other than OSR (e.g. socioeconomic or environmental factors may also have influenced the sex ratio at birth and the birth rate.

Adaptation, Physiological↗