Viability Selection Research Articles

The maintenance of single-locus polymorphism by maternal selection.

Population geneticists have long been interested in the ability of natural selection to maintain the levels of standing variation observed in natural populations. Here, we study the polymorphism-maintaining properties of maternal selection, in which the fitness of an individual is a function of its own and its mother’s genotype. Using a model proposed by Gavrilets, we first estimate the proportion of parameter/state space that preserves allelic variation, before investigating the construction of polymorphism over time through the joint action of mutation and selection. These two methods, the “parameter-space” and “constructionist” approaches, respectively, enable us to draw some general conclusions. We argue that, even though the proportion of parameter-state space allowing multiallele polymorphism is greater under maternal selection than under the standard model of constant viability selection, the former is, in fact, less likely to maintain large numbers of alleles. Nevertheless, variation that is balanced by maternal selection is likely to show elements of heterozygous advantage and be resistant to depletion by genetic drift. We observe that the population mean fitness frequently decreases after the successful invasion of a new mutation, but such declines are usually temporary.

Sexual size and shape dimorphism and allometric scaling patterns in head traits in the New Zealand common gecko Woodworthia maculatus

Sexual dimorphism in shape and size is widespread across animal taxa and arises when natural or sexual selection operates differently on the sexes. Male and female common geckos (Woodworthia maculatus; formerly Hoplodactylus maculatus) in New Zealand do not appear to experience different viability selection pressure, nor do males appear to be under intense pre-copulatory sexual selection. It was therefore predicted that this species would be sexually monomorphic with regard to body size and the size and shape of the head. In line with the prediction, there was no sexual difference in head width, depth, or length or in lateral head shape. However, contrary to prediction, males had a larger body and lateral head size than females. This study suggests that males, at least on Maud Island, NZ, might be under stronger pre-copulatory sexual selection than previously recognized and thus have evolved larger heads (i.e. lateral head size) for use in male combat for females. Allometric scaling patterns do not differ between the sexes and suggest that head width and depth are under directional selection whereas lateral head size is under stabilizing selection. Diet ecology – an agent of natural selection common to both sexes – is likely largely responsible for the observed patterns of head size and shape and the lack of sexual dimorphism in them.

The interpretation of selection coefficients.

Evolutionary biologists have an array of powerful theoretical techniques that can accurately predict changes in the genetic composition of populations. Changes in gene frequencies and genetic associations between loci can be tracked as they respond to a wide variety of evolutionary forces. However, it is often less clear how to decompose these various forces into components that accurately reflect the underlying biology. Here, we present several issues that arise in the definition and interpretation of selection and selection coefficients, focusing on insights gained through the examination of selection coefficients in multilocus notation. Using this notation, we discuss how its flexibility-which allows different biological units to be identified as targets of selection-is reflected in the interpretation of the coefficients that the notation generates. In many situations, it can be difficult to agree on whether loci can be considered to be under "direct" versus "indirect" selection, or to quantify this selection. We present arguments for what the terms direct and indirect selection might best encompass, considering a range of issues, from viability and sexual selection to kin selection. We show how multilocus notation can discriminate between direct and indirect selection, and describe when it can do so.

Ant sperm storage organs do not have phenoloxidase constitutive immune activity

The prophenoloxidase system (proPO-AS) is a primordial constituent of insect innate immunity. Its broad action spectrum, rapid response time, and cytotoxic by-products induced by phenoloxidase (PO) production contribute to the effective clearing of invading pathogens. However, such immune reactions may not be optimal for insect organs that evolved to have mutualistic interactions with non-self-cells. Ant queens are long-lived, but only mate early in adult life and store the sperm in a specialized organ, the spermatheca. They never re-mate so their life-time reproductive success is ultimately sperm-limited, which maintains strong selection for high sperm viability before and after storage. The proPO-AS may therefore be inappropriate for the selective clearing of sexually transmitted infections, as it might also target sperm cells that cannot be replaced.We measured PO enzymatic activity in the sperm storage organs of three ant species before and after mating. Our data show that no PO is produced in the sperm storage organs, relative to other somatic tissues as controls, and that these negative results are not due to non-detection in small volumes as non-immune-relevant catalase activity in single spermatheca fluid samples of both virgin and mated queens was significant. The lack of PO activity in sperm storage organs across three different ant species may represent an evolutionarily conserved adaptation to life-long sperm storage by ant queens. We expect that PO activity will be similarly suppressed in queen spermathecae of other eusocial Hymenoptera (bees and wasps) and, more generally, of insect females that store sperm for long periods.

An experimental test of density-dependent selection on temperament traits of activity, boldness and sociability.

Temperament traits are seen in many animal species, and recent evolutionary models predict that they could be maintained by heterogeneous selection. We tested this prediction by examining density-dependent selection in juvenile common lizards Zootoca vivipara scored for activity, boldness and sociability at birth and at the age of 1 year. We measured three key life-history traits (juvenile survival, body growth rate and reproduction) and quantified selection in experimental populations at five density levels ranging from low to high values. We observed consistent individual differences for all behaviours on the short term, but only for activity and one boldness measure across the first year of life. At low density, growth selection favoured more sociable lizards, whereas viability selection favoured less active individuals. A significant negative correlational selection on activity and boldness existed for body growth rate irrespective of density. Thus, behavioural traits were characterized by limited ontogenic consistency, and natural selection was heterogeneous between density treatments and fitness traits. This confirms that density-dependent selection plays an important role in the maintenance of individual differences in exploration-activity and sociability.

Impacts of early viability selection on management of inbreeding and genetic diversity in conservation.

Maintaining genetic diversity is a crucial goal of intensive management of threatened species, particularly for those populations that act as sources for translocation or re-introduction programmes. Most captive genetic management is based on pedigrees and a neutral theory of inheritance, an assumption that may be violated by selective forces operating in captivity. Here, we explore the conservation consequences of early viability selection: differential offspring survival that occurs prior to management or research observations, such as embryo deaths in utero. If early viability selection produces genotypic deviations from Mendelian predictions, it may undermine management strategies intended to minimize inbreeding and maintain genetic diversity. We use empirical examples to demonstrate that straightforward approaches, such as comparing litter sizes of inbred vs. noninbred breeding pairs, can be used to test whether early viability selection likely impacts estimates of inbreeding depression. We also show that comparing multilocus genotype data to pedigree predictions can reveal whether early viability selection drives systematic biases in genetic diversity, patterns that would not be detected using pedigree-based statistics alone. More sophisticated analysis combining genomewide molecular data with pedigree information will enable conservation scientists to test whether early viability selection drives deviations from neutrality across wide stretches of the genome, revealing whether this form of selection biases the pedigree-based statistics and inference upon which intensive management is based.

Geographic variation of life‐history traits in the sand lizard,Lacerta agilis: testing Darwin's fecundity‐advantage hypothesis

The fecundity-advantage hypothesis (FAH) explains larger female size relative to male size as a correlated response to fecundity selection. We explored FAH by investigating geographic variation in female reproductive output and its relation to sexual size dimorphism (SSD) in Lacerta agilis, an oviparous lizard occupying a major part of temperate Eurasia. We analysed how sex-specific body size and SSD are associated with two putative indicators of fecundity selection intensity (clutch size and the slope of the clutch size-female size relationship) and with two climatic variables throughout the species range and across two widespread evolutionary lineages. Variation within the lineages provides no support for FAH. In contrast, the divergence between the lineages is in line with FAH: the lineage with consistently female-biased SSD (L. a. agilis) exhibits higher clutch size and steeper fecundity slope than the lineage with an inconsistent and variable SSD (L. a. exigua). L. a. agilis shows lower offspring size (egg mass, hatchling mass) and higher clutch mass relative to female mass than L. a. exigua, that is both possible ways to enhance offspring number are exerted. As the SSD difference is due to male size (smaller males in L. a. agilis), fecundity selection favouring larger females, together with viability selection for smaller size in both sexes, would explain the female-biased SSD and reproductive characteristics of L. a. agilis. The pattern of intraspecific life-history divergence in L.agilis is strikingly similar to that between oviparous and viviparous populations of a related species Zootoca vivipara. Evolutionary implications of this parallelism are discussed.

Darwinian balancing selection: predation counters sexual selection in a wild insect.

The potential viability costs of sexually selected traits are central to hypotheses about the evolution of exaggerated traits. Estimates of these costs in nature can come from selection analyses using multiple components of fitness during the same time frame. For a population of tree crickets (Oecanthus nigricornis: Gryllidae), we analyzed viability and sexual selection on male traits by comparing Oecanthus prey of a solitary wasp to those that survived, and comparing mating individuals to solitary males. We measured forewing width (sexually size dimorphic and used for singing), head width, pronotum length, and size of hind jumping legs as potential targets of selection. Supporting the hypothesis that sexually selected traits have viability costs, we found that significant directional sexual selection for wider heads was opposed by significant viability selection for narrower heads. Nonlinear selection revealed that individuals with wide heads and small legs were most attractive, but individuals with narrow heads, large legs, and intermediate pronotum length were most likely to survive. Successful mating may put males at greater risk of predation, especially if copulation per se is risky. Such balancing selection in tree crickets may have constrained the evolution of sexual dimorphism in head size-a condition seen in other gryllids and orthopterans.

Inheritance of high-resolution melting profiles in assays targeting single nucleotide polymorphisms in protein-coding sequences of the Pacific oyster Crassostrea gigas: Implications for parentage assignment of experimental and commercial broodstocks

Abstract Single-nucleotide polymorphisms (SNPs) have become markers of choice in genetic studies and may be assayed by a variety of methods. For purposes of confirming pedigrees of experimental and commercial broodstocks of the Pacific oyster Crassostrea gigas , we developed PCR primers for exonic amplicons, ranging in size from 61 to 165 base pairs (average 95 bp) and high-resolution melting (HRM) assays for a set of 53 coding SNPs, which were previously identified from EST sequences and mapped in families. We define as canonical the three HRM profiles corresponding to the two homozygotes and the heterozygote expected at the target SNP (e.g. AA, GG, AG or AA, CC, AC), with variation at no other site in the PCR amplicon. We summarize data on Mendelian inheritance of HRM profiles in four, large, full-sib progenies from wild-caught parents and in 16 families with smaller numbers of progeny, a dataset of 24,065 HRM phenotypes. Not surprisingly, these family analyses confirm Mendelian inheritance of canonical HRM profiles, while showing evidence for non-amplifying null alleles and distortions of transmission ratios that can be ascribed to early viability selection. Unexpectedly, these family analyses reveal evidence for heritable, non-canonical HRM profiles, which we further describe. Non-canonical HRM phenotypes are found at 40 of the 53 markers but comprise only 5.37% of all phenotypes in our dataset (whereas technical artifacts account for only 0.4% of phenotypes and measured genotyping error from replicates is just 0.2%). Cloning and sequencing of 142, non-canonical HRM haplotypes, at 26 loci, reveal polymorphism at up to four sites besides the target nucleotide. Thus, HRM assays reveal extensive haplotype diversity within exons; interpreted correctly, this additional phenotypic variation increases the allelic diversity and power of parentage assignment for these Type-I markers.

Litter sizes of Daurian ground squirrels peak at intermediate body sizes

Litter size and body size of animals may coevolve under the concomitant pressures of sexual selection, fecundity selection, and viability selection. Studies have demonstrated the positive relationship between body size and litter size, consistent with Darwin's fecundity advantage of large body size. However, the counterbalancing selection hypothesis predicts fecundity selection would result in a positive correlation between litter size and body size initially, whereas the opposite pressure by viability selection would decrease litter size with further increasing body size beyond a threshold size. Moreover, the reproduction senescence hypothesis predicts that litter size of old, large females would decline with deteriorating body conditions. In this study, we tested the predictions of the counterbalancing selection hypothesis and the reproduction senescence hypothesis concerning the quadratic relationship between body size and litter size in Daurian ground squirrels (Spermophilus dauricus). Litter size increased initially with increasing carcass weight of females, and then decreased with further increases in carcass weight, supporting the prediction of the counterbalancing hypothesis. However, litter size was not related to body condition index of females, and body conditions improved with increasing body weight, suggesting that the reproduction senescence hypothesis alone cannot explain the observed quadratic relationship between litter size and carcass weight of female S. dauricus.

Obesity-driven disruption of haematopoiesis and the bone marrow niche

Obesity markedly increases susceptibility to a range of diseases and simultaneously undermines the viability and fate selection of haematopoietic stem cells (HSCs), and thus the kinetics of leukocyte production that is critical to innate and adaptive immunity. Considering that blood cell production and the differentiation of HSCs and their progeny is orchestrated, in part, by complex interacting signals emanating from the bone marrow microenvironment, it is not surprising that conditions that disturb bone marrow structure inevitably disrupt both the numbers and lineage-fates of these key blood cell progenitors. In addition to the increased adipose burden in visceral and subcutaneous compartments, obesity causes a marked increase in the size and number of adipocytes encroaching into the bone marrow space, almost certainly disturbing HSC interactions with neighbouring cells, which include osteoblasts, osteoclasts, mesenchymal cells and endothelial cells. As the global obesity pandemic grows, the short-term and long-term consequences of increased bone marrow adiposity on HSC lineage selection and immune function remain uncertain. This Review discusses the differentiation and function of haematopoietic cell populations, the principal physicochemical components of the bone marrow niche, and how this environment influences HSCs and haematopoiesis in general. The effect of adipocytes and adiposity on HSC and progenitor cell populations is also discussed, with the goal of understanding how obesity might compromise the core haematopoietic system.

In search of the best methods for multivariate selection analysis

SummaryRegression is an important method for characterizing the form of natural selection from individual‐based data. Many kinds of regression analysis exist, but few are regularly employed in studies of natural selection. I provide an overview of some of the main underused types of regression analysis by applying them to test analyses of viability selection for lamb traits in Soay sheep (Ovis aries). This exercise highlights known problems with existing methods, uncovers some new ones and also reveals ways to harness underused methods to get around these problems.I first estimate selection gradients using generalized linear models, combined with recently published methods for obtaining quantitatively interpretable selection gradient estimates from arbitrary regression models of trait–fitness relationships. I then also apply generalized ridge regression, the lasso and projection‐pursuit regression, in each case also deriving selection gradients. I compare inferences of nonlinear selection by diagonalization of theγmatrix and by projection‐pursuit regression.Selection gradient estimates generally correspond across different regression methods. Although there is little evidence for nonlinear selection in the test data sets, very problematic aspects of the behaviour of analysis based on diagonalization of theγare apparent. In addition to better‐known problems, (i) the direction and magnitude of estimated major axes of quadratic selection are biased towards directions of phenotype that have little variance, and (ii) the magnitudes of selection of major axes of variance‐standardizedγare not themselves interpretable in any standardized way.While all regression‐based methods for analysis of selection have useful properties, projection‐pursuit regression seems to stand out. This method can (i) provide both dimensionality reduction, (ii) be the basis for inference of quantitatively interpretable selection gradients and (iii) by characterizing major axes of selection, rather than of linear or quadratic selection separately, provide biologically interpretable inference of nonlinear selection.

Parental provisioning in house wrens: effects of varying brood size and consequences for offspring

In biparental species, conflict between the sexes is expected when optimal levels of parental care differ between males and females. We studied food provisioning in house wrens (Troglodytes aedon) to test whether male provisioning is more strongly affected than female provisioning by brood size, because this should influence the marginal return on a male’s investment. To test this, we created broods of reduced and enlarged size, and found that per-nestling food delivery varied more strongly for males than for females in association with brood size and nestling age; males delivered more food per nestling to enlarged broods, and less to small broods, as nestlings grew and approached asymptotic size. Although parents delivered a greater amount of prey to larger broods, the amount of food per nestling was initially higher for nestlings in small broods, and the amount of food delivered early in nestling development, particularly by males, affected offspring body mass, survival to fledging, and recruitment to the breeding population. However, provisioning rates were negatively associated with prey size, suggesting a trade-off between prey quantity and size. Finally, parents provisioning at a high rate to broods of reduced size were less likely to return to breed, suggesting that they assessed the low return on their investment and dispersed. Although potential for sexual conflict in house wrens remains, our data suggest that its resolution does not involve negotiation over provisioning, possibly because selection for offspring viability favors heavy investment by both parents.

Adaptive fixation in two-locus models of stabilizing selection and genetic drift.

The relationship between quantitative genetics and population genetics has been studied for nearly a century, almost since the existence of these two disciplines. Here we ask to what extent quantitative genetic models in which selection is assumed to operate on a polygenic trait predict adaptive fixations that may lead to footprints in the genome (selective sweeps). We study two-locus models of stabilizing selection (with and without genetic drift) by simulations and analytically. For symmetric viability selection we find that ∼16% of the trajectories may lead to fixation if the initial allele frequencies are sampled from the neutral site-frequency spectrum and the effect sizes are uniformly distributed. However, if the population is preadapted when it undergoes an environmental change (i.e., sits in one of the equilibria of the model), the fixation probability decreases dramatically. In other two-locus models with general viabilities or an optimum shift, the proportion of adaptive fixations may increase to >24%. Similarly, genetic drift leads to a higher probability of fixation. The predictions of alternative quantitative genetics models, initial conditions, and effect-size distributions are also discussed.

Gape-limited predators as agents of selection on the defensive morphology of an invasive invertebrate.

Invasive species have widespread and pronounced effects on ecosystems and adaptive evolution of invaders is often considered responsible for their success. Despite the potential importance of adaptation to invasion, we still have limited knowledge of the agents of natural selection on invasive species. Bythotrephes longimanus, a cladoceran zooplankton, invaded multiple Canadian Shield lakes over the past several decades. Bythotrephes have a conspicuous caudal process (tail spine) that provides a morphological defense against fish predation. We measured viability selection on the longest component of the Bythotrephes spine, the distal spine segment, through a comparison of the lengths of first and second instar Bythotrephes collected from lakes differing in the dominance of gape-limited predation (GLP) and nongape-limited predation (NGLP) by fish. We found that natural selection varied by predator gape-limitation, with strong selection (selection intensity: 0.20-0.79) for increased distal spine length in lakes dominated by GLP, and no significant selection in lakes dominated by NGLP. Further, distal spine length was 17% longer in lakes dominated by GLP, suggesting the possibility of local adaptation. As all study lakes were invaded less than 20 years prior to our collections, our results suggest rapid divergence in defensive morphology in response to selection from fish predators.

Fitness consequences of environmental conditions at different life stages in a long-lived vertebrate.

The predictive adaptive response (PAR) hypothesis proposes that animals adjust their physiology and developmental trajectory during early life in anticipation of their future environments. Accordingly, when environmental conditions in early life match environmental conditions during adulthood, individual fitness should be greater. Here, we test this hypothesis in a long-lived mammal, the roe deer, using data from two contrasting populations, intensively monitored for more than 35 years. In the highly productive site, the fitness of female roe deer increased with the quality of environment during adulthood and, contrary to predictions of PAR, individuals born in good conditions always outperformed those born under poor conditions. In the resource-limited site, the fitness of female roe deer born in poor years was better than those born in good conditions in poor years when the animals were adult, but not in good years. Although consistent with predictions of PAR, we showed that this pattern is likely to be a consequence of increased viability selection during the juvenile stage for animals born in poor years. While PARs are often advanced in evolutionary medicine, our findings suggest that detailed biological processes should be investigated before drawing conclusions about the existence of this phenomenon.

Contrasting patterns of selection on the size and coloration of a female plumage ornament in common yellowthroats

Females often possess ornaments that appear smaller and duller than homologous traits in males. These ornaments may arise as nonfunctional by-products of sexual selection in males and cause negative viability or fecundity selection in females in proportion to the cost of their production and maintenance. Alternatively, female ornaments may function as signals of quality that are maintained by sexual or social selection. In a 4-year study of 83 female common yellowthroats (Geothlypis trichas) and their 222 young, we found strong viability and fecundity selection on the yellow bib, a carotenoid-based plumage ornament that is a target of sexual selection in males. Females with larger bibs were older, larger and more fecund than females with smaller bibs. However, bib size positively covaried with bib total brightness and carotenoid chroma, aspects of bib coloration that were under negative viability and fecundity selection. Females with more colourful bibs laid fewer eggs in their first clutch, were more likely to suffer total brood loss due to predation and were less likely to return to the study area. Selection against bib coloration limits the value of bib size as a quality indicator in females and may constrain the elaboration of bib attributes in males.

Sensory drive speciation and patterns of variation at selectively neutral genes

Speciation by sensory drive can occur if divergent adaptation of sensory systems causes rapid evolution of mating traits and the resulting development of assortative mating. Previous theoretical studies have shown that sensory drive can cause rapid divergent adaptive evolution from one to two phenotypes. In this study, we examined two topics: the possibility of adaptive radiation by sensory drive from one to more than two phenotypes and the relationships of patterns of variation at selectively neutral genes to levels of viability selection, habitat and mating preferences and migration. We conducted individual-based simulations assuming a sensory trait and a mating trait controlled by a small number of loci. We found that adaptive radiation is possible when the number of loci controlling the sensory trait is small; the levels of viability selection, habitat and mating preferences are intermediate; and the emigration rate is high. We also found that emigration rates as well as the levels of habitat and mating preferences are related to F ST values at neutral loci, but F ST proved to be insensitive to a small change in the number of loci controlling the mating trait. This suggests that an estimation of the past population history is possible without an accurate genetic model.

Emerging infectious disease selects for darker plumage coloration in greenfinches

Outbreaks of emerging infectious disease offer a unique chance to study viability selection in action in short time windows. Finch trichomonosis, caused by a protozoan Trichomonas gallinae emerged in Great Britain in 2005 and led to epidemic mortality and a significant population decline of greenfinches, Carduelis chloris in UK and Northern European countries in subsequent years. We recorded covariation between plumage characteristics and trichomonosis-induced mortality among wild-caught greenfinches brought into captivity in Tartu, Estonia. Occurrence of fault bars (markers of stressful conditions experienced during feather growth) on tail feathers was five times higher among the dead birds than among survivors. Black (eumelanotic) compartments of tail feathers of survivors were on average 22 % darker than feathers of dead birds. Such pattern is best explained by proposed pleiotropic effects of genes involved in eumelanin production on immune function. These findings suggest that melanin-based coloration can evolve via mechanisms that are independent of visual information provided by the pigment.

An improved method to obtain novel mutants in Cucurbita pepo by pollen viability

A new genetic resource for Cucurbita pepo has been developed with chemically induced mutagenesis. The seeds of the zucchini cultivar MU-CU16 were treated with 40mM–80mM ethyl methanesulfonate (EMS), reaching high germination rates between 70 and 85%. However, most plants of those M1 populations did not produce offspring, and the fertility rates were lower in plants treated with higher concentrations of EMS. Once we established that visual flower abnormality rates were not sufficient to explain low fruit yield, pollen viability was analysed with fluorochromatic reaction. Compared with untreated plants, treatment with EMS produced a substantial decrease in pollen viability, and only the group of plants with pollen viability rates higher than 45% yielded nearly 70% of fruits with seeds. Therefore, the main issues to be addressed for developing mutant lines in this species are to increase the number of mutations in the genome and to increase the number of mutant lines with sufficient fertility. In this case, the early plantlet selection for high pollen viability carried out as part of this work represents a useful tool for use in future breeding programs by mutagenesis, allowing an increase of up to 40% in the production of mutant lines for a dosage of 65mM EMS.