Effect of migration and environmental heterogeneity on the maintenance of quantitative genetic variation: a simulation study

The paradox of high genetic variation observed in traits under stabilizing selection is a long‐standing problem in evolutionary theory, as mutation rates appear too low to explain observed levels of standing genetic variation under classic models of mutation–selection balance. Spatially or temporally heterogeneous environments can maintain more standing genetic variation within populations than homogeneous environments, but it is unclear whether such conditions can resolve the above discrepancy between theory and observation. Here, we use individual‐based simulations to explore the effect of various types of environmental heterogeneity on the maintenance of genetic variation (V_A) for a quantitative trait under stabilizing selection. We find that V_A is maximized at intermediate migration rates in spatially heterogeneous environments and that the observed patterns are robust to changes in population size. Spatial environmental heterogeneity increased variation by as much as 10‐fold over mutation–selection balance alone, whereas pure temporal environmental heterogeneity increased variance by only 45% at max. Our results show that some combinations of spatial heterogeneity and migration can maintain considerably more variation than mutation–selection balance, potentially reconciling the discrepancy between theoretical predictions and empirical observations. However, given the narrow regions of parameter space required for this effect, this is unlikely to provide a general explanation for the maintenance of variation. Nonetheless, our results suggest that habitat fragmentation may affect the maintenance of V_A and thereby reduce the adaptive capacity of populations.     

The nature of quantittative genetic variation revisited: Lessons from Drosophila bristles

Most characters that distinguish one individual from another, like height or weight, vary continuously in populations. Continuous variation of these ‘quantitative’ traits is due to the simultaneous segregation of multiple quantitative trait loci (QTLs) as well as environmental influences. A major challenge in human medicine, animal and plant breeding and evolutionary genetics is to identify QTLs and determine their genetic properties. Studies of the classic quantitative traits, abdominal and sternopleural bristle numbers of Drosophila, have shown that: (1) many loci have small effects on bristle number, but a few have large effects and cause most of the genetic variation; (2) ‘candidate’ loci involved in bristle development often have large quantitative effects on bristle number; and (3) alleles at QTLs affecting bristle number have variable degrees of dominance, interact with each other, and affect other quantitative traits, including fitness. Lessons learned from this model system will be applicable to studies of the genetic basis of quantitative variation in other species.     

Mitochondrial haplotype does not affect sperm velocity in the zebra finch Taeniopygia guttata

Mitochondrial DNA (mtDNA) variation has been suggested as a possible cause of variation in male fertility because sperm activity is tightly coupled to mitochondrial oxidative phosphorylation and ATP production, both of which are sensitive to mtDNA mutations. Since male‐specific phenotypes such as sperm have no fitness consequences for mitochondria due to maternal mitochondrial (and mtDNA) inheritance, mtDNA mutations that are deleterious in males but which have negligible or no fitness effect in females can persist in populations. How often such mutations arise and persist is virtually unknown. To test whether there were associations between mtDNA variation and sperm performance, we haplotyped 250 zebra finches Taeniopygia guttata from a large pedigreed‐population and measured sperm velocity using computer‐assisted sperm analysis. Using quantitative genetic ‘animal’ models, we found no effect of mtDNA haplotype on sperm velocity. Therefore, there is no evidence that in this system mitochondrial mutations have asymmetric fitness effects on males and females, leading to genetic variation in male fertility that is blind to natural selection.     

QUANTITATIVE GENETICS IN PLANTS: THE EFFECT OF THE BREEDING SYSTEM ON GENETIC VARIABILITY

The expected effects of breeding system on quantitative genetic variation under various models for the maintenance of such variation are examined, with particular emphasis on the contrast between randomly mating and highly self-fertilizing populations. Estimates of quantitative genetic parameters from plant populations are reviewed. There is some evidence for reduced within-population genetic variance in highly inbreeding populations, compared with outbreeders, but more empirical work appears necessary. Although the estimate of the magnitude of the effect of breeding system is subject to considerable error, the reduction in genetic variance in inbreeding populations appears greater than expected if the variation were maintained by overdominance, or if it were due to neutral mutations. It is more consistent with models involving mutation-selection balance, although a rather larger reduction in genetic variance is estimated than is expected theoretically. We discuss some possible reasons for the lower level of genetic variance in selfers than is predicted by such models.     

Genetic variability under mutation selection balance

A fundamental problem in evolutionary genetics is understanding how high levels of genetic variation in quantitative traits are maintained in natural populations. Variation is removed by the natural selection of individuals with optimal phenotypes and is recovered by mutation; however, previous analyses had indicated that a mutation-selection balance was insufficient to maintain observed levels of genetic variation in these traits. Using more general models, however, it has recently been shown that it is indeed a sufficient mechanism. These models can be used to explore other phenomena in evolutionary biology.     

It takes two: Heritable male effects on reproductive timing but not clutch size in a wild bird population*

Within-population variation in the traits underpinning reproductive output has long been of central interest to biologists. Since they are strongly linked to lifetime reproductive success, these traits are expected to be subject to strong selection and, if heritable, to evolve. Despite the formation of durable pair bonds in many animal taxa, reproductive traits are often regarded as female-specific, and estimates of quantitative genetic variation seldom consider a potential role for heritable male effects. Yet reliable estimates of such social genetic effects are important since they influence the amount of heritable variation available to selection. Based on a 52-year study of a nestbox-breeding great tit (Parus major) population, we apply “extended” bivariate animal models in which the heritable effects of both sexes are modeled to assess the extent to which males contribute to heritable variation in seasonal reproductive timing (egg laying date) and clutch size, while accommodating the covariance between the two traits. Our analyses show that reproductive timing is a jointly expressed trait in this species, with (positively covarying) heritable variation for laydate being expressed in both members of a breeding pair, such that the total heritable variance is 50% larger than estimated by traditional models. This result was robust to explicit consideration of a potential male-biased environmental confound arising through sexually dimorphic dispersal. In contrast to laydate, males’ contribution to heritable variation in clutch size was limited. Our study thus highlights the contrasting extent of social determination for two major components of annual reproductive success, and emphasizes the need to consider the social context of what are often considered individual-level traits.     

Evolution in heterogeneous environments and the potential of maintenance of genetic variation in traits of adaptive significance

The maintenance of genetic variation in traits of adaptive significance has been a major dilemma of evolutionary biology. Considering the pattern of increased genetic variation associated with environmental clines and heterogeneous environments, selection in heterogeneous environments has been proposed to facilitate the maintenance of genetic variation. Some models examining whether genetic variation can be maintained, in heterogeneous environments are reviewed. Genetic mechanisms that constrain evolution in quantitative genetic traits indicate that genetic variation can be maintained but when is not clear. Furthermore, no comprehensive models have been developed, likely due to the genetic and environmental complexity of this issue. Therefore, I have suggested two empirical approaches to provide insight for future theoretical and empirical research. Traditional path analysis has been a very powerful approach for understanding phenotypic selection. However, it requires substantial information on the biology of the study system to construct a causal model and alternatives. Exploratory path analysis is a data driven approach that uses the statistical relationships in the data to construct a set of models. For example, it can be used for understanding phenotypic selection in different environments, where there is no prior information to develop path models in the different environments. Data from Brassica rapa grown in different nutrients indicated that selection changed in the different environments. Experimental evolutionary studies will provide direct tests as to when genetic variation is maintained.     

A POPULATION GENETIC THEORY OF CANALIZATION

Canalization is the suppression of phenotypic variation. Depending on the causes of phenotypic variation, one speaks either of genetic or environmental canalization. Genetic canalization describes insensitivity of a character to mutations, and the insensitivity to environmental factors is called environmental canalization. Genetic canalization is of interest because it influences the availability of heritable phenotypic variation to natural selection, and is thus potentially important in determining the pattern of phenotypic evolution. In this paper a number of population genetic models are considered of a quantitative character under stabilizing selection. The main purpose of this study is to define the population genetic conditions and constraints for the evolution of canalization. Environmental canalization is modeled as genotype specific environmental variance. It is shown that stabilizing selection favors genes that decrease environmental variance of quantitative characters. However, the theoretical limit of zero environmental variance has never been observed. Of the many ways to explain this fact, two are addressed by our model. It is shown that a “canalization limit” is reached if canalizing effects of mutations are correlated with direct effects on the same character. This canalization limit is predicted to be independent of the strength of stabilizing selection, which is inconsistent with recent experimental data (Sterns et al. 1995). The second model assumes that the canalizing genes have deleterious pleiotropic effects. If these deleterious effects are of the same magnitude as all the other mutations affecting fitness very strong stabilizing selection is required to allow the evolution of environmental canalization. Genetic canalization is modeled as an influence on the average effect of mutations at a locus of other genes. It is found that the selection for genetic canalization critically depends on the amount of genetic variation present in the population. The more genetic variation, the stronger the selection for canalizing effects. All factors that increase genetic variation favor the evolution of genetic canalization (large population size, high mutation rate, large number of genes). If genetic variation is maintained by mutation-selection balance, strong stabilizing selection can inhibit the evolution of genetic canalization. Strong stabilizing selection eliminates genetic variation to a level where selection for canalization does not work anymore. It is predicted that the most important characters (in terms of fitness) are not necessarily the most canalized ones, if they are under very strong stabilizing selection (k > 0.2V_e). The rate of decrease of mutational variance V_m is found to be less than 10% of the initial V_m. From this result it is concluded that characters with typical mutational variances of about 10^–3 V_e are in a metastable state where further evolution of genetic canalization is too slow to be of importance at a microevolutionary time scale. The implications for the explanation of macroevolutionary patterns are discussed.     

Daily Energy Balance and Protein Gain Among <Emphasis Type="Italic">Pan troglodytes verus</Emphasis> in the Taï National Park,Côte d’Ivoire

Energy balance and protein gain contribute significantly to an animal’s survival. Although data are available for certain species in captive settings, there is little information on these factors for primates living in their natural environments. In this preliminary study, we combined detailed behavioral, phonological, and chemical data for a well habituated chimpanzee community from the Taï National Park, Côte d’Ivoire, with estimates of energy gain and expenditure from captive chimpanzees and humans to investigate how energy balance and protein gain across age-sex categories are affected by seasonal variations in food availability and how chimpanzees correspondingly alter their feeding and daily journey length (DJL). Comparisons between fruiting seasons characterized by varying quantities and qualities of available food revealed that food quality had the largest effect on individual energy balance and protein gain. Within given fruit seasons, energy balance and protein gain did not vary among age-sex categories. However, there was, variation across seasons among adult males and young of both sexes, but not among adult females. Our study revealed important effects of periods of food scarcity to which chimpanzees reacted by reducing their DJL and increasing their feeding time.     

Construction of a multiple fluorescence labelling system for use in co-invasion studies of Listeria monocytogenes

Background  

Existing virulence models are often difficult to apply for quantitative comparison of invasion potentials of Listeria monocytogenes. Well-to-well variation between cell-line based in vitro assays is practically unavoidable, and variation between individual animals is the cause of large deviations in the observed capacity for infection when animal models are used.     

The contribution of animal models to the study of obesity

Obesity results from prolonged imbalance of energy intake and energy expenditure. Animal models have provided a fundamental contribution to the historical development of understanding the basic parameters that regulate the components of our energy balance. Five different types of animal model have been employed in the study of the physiological and genetic basis of obesity. The first models reflect single gene mutations that have arisen spontaneously in rodent colonies and have subsequently been characterized. The second approach is to speed up the random mutation rate artificially by treating rodents with mutagens or exposing them to radiation. The third type of models are mice and rats where a specific gene has been disrupted or over-expressed as a deliberate act. Such genetically-engineered disruptions may be generated through the entire body for the entire life (global transgenic manipulations) or restricted in both time and to certain tissue or cell types. In all these genetically-engineered scenarios, there are two types of situation that lead to insights: where a specific gene hypothesized to play a role in the regulation of energy balance is targeted, and where a gene is disrupted for a different purpose, but the consequence is an unexpected obese or lean phenotype. A fourth group of animal models concern experiments where selective breeding has been utilized to derive strains of rodents that differ in their degree of fatness. Finally, studies have been made of other species including non-human primates and dogs. In addition to studies of the physiological and genetic basis of obesity, studies of animal models have also informed us about the environmental aspects of the condition. Studies in this context include exploring the responses of animals to high fat or high fat/high sugar (Cafeteria) diets, investigations of the effects of dietary restriction on body mass and fat loss, and studies of the impact of candidate pharmaceuticals on components of energy balance. Despite all this work, there are many gaps in our understanding of how body composition and energy storage are regulated, and a continuing need for the development of pharmaceuticals to treat obesity. Accordingly, reductions in the use of animal models, while ethically desirable, will not be feasible in the short to medium term, and indeed an expansion in activity using animal models is anticipated as the epidemic continues and spreads geographically.     

Tail colour signals performance in blue tit nestlings

Indirect sexual selection arises when reproductive individuals choose their mates based on heritable ornaments that are genetically correlated to fitness. Evidence for genetic associations between ornamental colouration and fitness remains scarce. In this study, we investigate the quantitative genetic relationship between different aspects of tail structural colouration (brightness, hue and UV chroma) and performance (cell‐mediated immunity, body mass and wing length) in blue tit (Cyanistes caeruleus) nestlings. In line with previous studies, we find low heritability for structural colouration and moderate heritability for performance measures. Multivariate animal models show positive genetic correlations between the three measures of performance, indicating quantitative genetic variation for overall performance, and tail brightness and UV chroma, two genetically independent colour measures, are genetically correlated with performance (positively and negatively, respectively). Our results suggest that mate choice based on independent aspects of tail colouration can have fitness payoffs in blue tits and provide support for the indirect benefits hypothesis. However, low heritability of tail structural colouration implies that indirect sexual selection on mate choice for this ornament will be a weak evolutionary force.     

Analysis of feed intake and energy balance of high-yielding first lactating Holstein cows with fixed and random regression models

At the dairy research farm Karkendamm, the individual roughage intake was measured since 1 September 2005 using a computerised scale system to estimate daily energy balances as the difference between energy intake and calculated energy requirements for lactation and maintenance. Data of 289 heifers with observations between the 11th and 180th day of lactation over a period of 487 days were analysed. Average energy-corrected milk yield, feed intake, live weight and energy balance were 31.8kg, 20.6kg, 584 kg and 13.6 MJ NEL (net energy lactation), respectively, per day. Fixed and random regression models were used to estimate repeatabilities, correlations between cow effects and genetic parameters. The resulting genetic correlations in different lactation stages demonstrate that feed intake and energy balance at the beginning and the middle of lactation are genetically different traits. Heritability of feed intake is low with h2=0.06 during the first days after parturition and increases in the middle of lactation, whereas the energy balance shows the highest heritability with h2=0.34 in the first 30 days of lactation. Genetic correlations between energy balance and feed intake and milk yield, respectively, illustrate that energy balance depends more on feed intake than on milk yield. Genetic correlation between body condition score and energy balance decreases rapidly within the first 100 days of lactation. Hence, to avoid negative effects on health and reproduction as consequences of strong energy deficits at the beginning of lactation, the energy balance itself should be measured and used as a selection criterion in this lactation stage. Since the number of animals is rather small for a genetic analysis, the genetic parameters have to be evaluated on a more comprehensive dataset.     

Genetic association between body energy measured throughout lactation and fertility in dairy cattle

The objective of this study was to quantify the genetic association of body energy assessed throughout lactation with a cow's fertility. Nine direct and indirect body energy traits were defined at different stages of lactation. Four were daily records of energy balance, energy content, cumulative effective energy (CEE) and body condition score (BCS) calculated between lactation days 4 and 311. The other five traits included duration of negative energy balance (DNEB), rate of recovery during DNEB (RNEB), sum of negative energy balance (SNEB), nadir of energy content (NEC) and number of days from calving to NEC. Of these traits, energy balance, DNEB, RNEB and SNEB were primarily based on individual cow feed intake and milk yield, and considered direct measures of body energy. The other traits were calculated from body lipid and protein changes, predicted from BCS and live weight profiles, and were considered indirect measures of body energy. Fertility was defined by number of days between calving and commencement of luteal activity (DLA), first observed oestrus (DH) and conception (DC), and number of services per conception. A total of 957 cows in their first four lactations were considered in the study. Genetic models fitted cubic splines to define longitudinal traits (energy balance, energy content, CEE and BCS) and calculate heritability and genetic correlation with fertility. Daily heritability estimate ranges were 0.10 to 0.34, 0.35 to 0.61, 0.32 to 0.53 and 0.24 to 0.56 for energy balance, energy content, CEE and BCS, respectively, and, in most cases, tended to increase towards the middle of lactation and remain relatively stable thereafter. Of the other body energy traits, heritability of NEC (0.44) was the most notable. Statistically significant (P < 0.05) genetic correlations of DH with daily energy balance, energy content, CEE and BCS ranged from -0.16 to -0.28, -0.35 to -0.48, -0.16 to -0.26 and -0.37 to -0.44, respectively. For DC, respective estimates were -0.28 to -0.64, -0.37 to -0.60, -0.30 to -0.48 and -0.29 to -0.53. For DLA, they ranged from -0.47 to -0.56 with energy content and from -0.50 to -0.74 with BCS. Of special interest was the genetic correlation of NEC with DH (-0.54) and DC (-0.48). Results suggest that indirect measures of body energy have the strongest genetic association with cow fertility. NEC and early lactation (circa day 50) BCS and energy content are the most useful traits for selection in terms of the correlated improvement in a cow's capacity to resume her reproductive activity post partum.     

Local adaptation versus historical isolation as sources of melanin‐based coloration in the white‐throated thrush Turdus assimilis

Local adaptation seems to be one of the causes of variation in melanin‐based colors in bird plumages, related mainly to the heterogeneity of the environmental conditions along the distribution of a species. Based on comparisons of genetic (mtDNA sequences), ecological (niche models), and quantitative colorimetric data, we explored variation in plumage coloration of the white‐throated thrush Turdus assimilis, a Mesoamerican species whose dorsal color varies from brown (northern and central Mexico) to dark gray (southern Mexico and Central America). Our results suggest the existence of two major patterns of coloration in this bird, which are congruent with the genetic structure, and comparisons of ecological niche models showed that population's niches were more similar than expected by chance, suggesting that color variation in plumage of T. assimilis is not consequence of local adaptation to different environmental conditions. Our results also showed that a greater geographic distance between populations is correlated with greater colorimetric differences, suggesting that color variation in T. assimilis may be consequence of historical isolation.     

Are QST–FST comparisons for natural populations meaningful?

Comparisons between putatively neutral genetic differentiation amongst populations, F_ST, and quantitative genetic variation, Q_ST, are increasingly being used to test for natural selection. However, we find that approximately half of the comparisons that use only data from wild populations confound phenotypic and genetic variation. We urge the use of a clear distinction between narrow‐sense Q_ST, which can be meaningfully compared with F_ST, and phenotypic divergence measured between populations, P_ST, which is inadequate for comparisons in the wild. We also point out that an unbiased estimate of Q_ST can be found using the so‐called ‘animal model’ of quantitative genetics.     

Population structure in the barn swallow,Hirundo rustica: a comparison between neutral DNA markers and quantitative traits

Local adaptation to variable environments can generate clinal variation in morphological traits. Alternatively, similar patterns of clinal variation may be generated simply as a result of genetic drift/migration balance. Teasing apart these different processes is a continuing focus in evolutionary ecology. We compare genetic differentiation at molecular loci and quantitative traits to analyse the effect of these different processes in a morphological latitudinal cline of the barn swallow, Hirundo rustica, breeding across Europe. The results obtained show no structuring at neutral microsatellite loci, which contrasts with positive structuring at five quantitative morphometric traits. This supports the hypothesis that the observed morphometric cline in barn swallows is the result of selection acting in a spatially heterogeneous environment. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 306–314.     

The genetic basis of female multiple mating in a polyandrous livebearing fish

The widespread occurrence of female multiple mating (FMM) demands evolutionary explanation, particularly in the light of the costs of mating. One explanation encapsulated by “good sperm” and “sexy‐sperm” (GS‐SS) theoretical models is that FMM facilitates sperm competition, thus ensuring paternity by males that pass on genes for elevated sperm competitiveness to their male offspring. While support for this component of GS‐SS theory is accumulating, a second but poorly tested assumption of these models is that there should be corresponding heritable genetic variation in FMM – the proposed mechanism of postcopulatory preferences underlying GS‐SS models. Here, we conduct quantitative genetic analyses on paternal half‐siblings to test this component of GS‐SS theory in the guppy (Poecilia reticulata), a freshwater fish with some of the highest known rates of FMM in vertebrates. As with most previous quantitative genetic analyses of FMM in other species, our results reveal high levels of phenotypic variation in this trait and a correspondingly low narrow‐sense heritability (h² = 0.11). Furthermore, although our analysis of additive genetic variance in FMM was not statistically significant (probably owing to limited statistical power), the ensuing estimate of mean‐standardized additive genetic variance (I_A = 0.7) was nevertheless relatively low compared with estimates published for life‐history traits across a broad range of taxa. Our results therefore add to a growing body of evidence that FMM is characterized by relatively low additive genetic variation, thus apparently contradicting GS‐SS theory. However, we qualify this conclusion by drawing attention to potential deficiencies in most designs (including ours) that have tested for genetic variation in FMM, particularly those that fail to account for intersexual interactions that underlie FMM in many systems.     

Combining quantitative trait loci analysis with physiological models to predict genotype‐specific transpiration rates

Transpiration is controlled by evaporative demand and stomatal conductance (g_s), and there can be substantial genetic variation in g_s. A key parameter in empirical models of transpiration is minimum stomatal conductance (g₀), a trait that can be measured and has a large effect on g_s and transpiration. In Arabidopsis thaliana, g₀ exhibits both environmental and genetic variation, and quantitative trait loci (QTL) have been mapped. We used this information to create a genetically parameterized empirical model to predict transpiration of genotypes. For the parental lines, this worked well. However, in a recombinant inbred population, the predictions proved less accurate. When based only upon their genotype at a single g₀ QTL, genotypes were less distinct than our model predicted. Follow‐up experiments indicated that both genotype by environment interaction and a polygenic inheritance complicate the application of genetic effects into physiological models. The use of ecophysiological or ‘crop’ models for predicting transpiration of novel genetic lines will benefit from incorporating further knowledge of the genetic control and degree of independence of core traits/parameters underlying g_s variation.     

Mutations in the bovineABCG2 and the ovineMSTN gene added to the few quantitative trait nucleotides identified in farm animals: a mini-review

The progress in molecular genetics in animal breeding is moderately effective as compared to traditional animal breeding using quantitative genetic approaches. There is an extensive disparity between the number of reported quantitative trait loci (QTLs) and their linked genetic variations in cattle, pig, and chicken. The identification of causative mutations affecting quantitative traits is still very challenging and hampered by the cloudy relationship between genotype and phenotype. There are relatively few reports in which a successful identification of a causative mutation for an animal production trait was demonstrated. The examples that have attracted considerable attention from the animal breeding community are briefly summarized and presented in a table. In this mini-review, the recent progress in mapping quantitative trait nucleotides (QTNs) are reviewed, including theABCG2 gene mutation that underlies a QTL for fat and protein content and the ovineMSTN gene mutation that causes muscular hypertrophy in Texel sheep. It is concluded that the progress in molecular genetics might facilitate the elucidation of the genetic architecture of QTLs, so that also the high-hanging fruits can be harvested in order to contribute to efficient and sustainable animal production.