QUANTITATIVE GENETICS OF MORPHOLOGICAL DIFFERENTIATION IN PEROMYSCUS. II. ANALYSIS OF SELECTION AND DRIFT

The hypothesis that the morphological divergence of local populations of Peromyscus is due to random genetic drift was evaluated by testing the proportionality of the among-locality covariance matrix, L, and the additive genetic covariance matrix, G. Overall, significant proportionality of L? and ? was not observed, indicating the evolutionary divergence of local populations does not result from random genetic drift. The forces of selection needed to differentiate three taxa of Peromyscus were reconstructed to examine the divergence of species and subspecies. The selection gradients obtained illustrate the inadequacy of univariate analyses of selection by finding that some characters evolve in the direction opposite to the force of selection acting directly on them. A retrospective selection index was constructed using the estimated selection gradients, and truncation selection on this index was used to estimate the minimum selective mortality per generation required to produce the observed change. On any of the time scales used, the proportion of the population that would need to be culled was quite low, the greatest being of the same order of magnitude as the selective intensities observed in extant natural populations. Thus, entirely plausible intensities of directional natural selection can produce species-level differences in a period of time too short to be resolved in the fossil record.     

PHYLOGENETIC ANALYSIS OF PHENOTYPIC COVARIANCE STRUCTURE. I. CONTRASTING RESULTS FROM MATRIX CORRELATION AND COMMON PRINCIPAL COMPONENT ANALYSES

Applications of quantitative techniques to understanding macroevolutionary patterns typically assume that genetic variances and covariances remain constant. That assumption is tested among 28 populations of the Phyllotis darwini species group (leaf-eared mice). Phenotypic covariances are used as a surrogate for genetic covariances to allow much greater phylogenetic sampling. Two new approaches are applied that extend the comparative method to multivariate data. The efficacy of these techniques are compared, and their sensitivity to sampling error examined. Pairwise matrix correlations of correlation matrices are consistently very high (> 0.90) and show no significant association between matrix similarity and phylogenetic relatedness. Hierarchical decomposition of common principal component (CPC) analyses applied to each clade in the phylogeny rejects the hypothesis that common principal component structure is shared in clades more inclusive than subspecies. Most subspecies also lack a common covariance structure as described by the CPC model. The hypothesis of constant covariances must be rejected, but the magnitudes of divergence in covariance structure appear to be small. Matrix correlations are very sensitive to sampling error, while CPC is not. CPC is a powerful statistical tool that allows detailed testing of underlying patterns of covariation.     

TYPE I ERROR RATES FOR TESTING GENETIC DRIFT WITH PHENOTYPIC COVARIANCE MATRICES: A SIMULATION STUDY

Studies of evolutionary divergence using quantitative genetic methods are centered on the additive genetic variance–covariance matrix ( G ) of correlated traits. However, estimating G properly requires large samples and complicated experimental designs. Multivariate tests for neutral evolution commonly replace average G by the pooled phenotypic within‐group variance–covariance matrix ( W ) for evolutionary inferences, but this approach has been criticized due to the lack of exact proportionality between genetic and phenotypic matrices. In this study, we examined the consequence, in terms of type I error rates, of replacing average G by W in a test of neutral evolution that measures the regression slope between among‐population variances and within‐population eigenvalues (the Ackermann and Cheverud [AC] test) using a simulation approach to generate random observations under genetic drift. Our results indicate that the type I error rates for the genetic drift test are acceptable when using W instead of average G when the matrix correlation between the ancestral G and P is higher than 0.6, the average character heritability is above 0.7, and the matrices share principal components. For less‐similar G and P matrices, the type I error rates would still be acceptable if the ratio between the number of generations since divergence and the effective population size (t/N_e) is smaller than 0.01 (large populations that diverged recently). When G is not known in real data, a simulation approach to estimate expected slopes for the AC test under genetic drift is discussed.     

POPULATION STRUCTURE OF MORPHOLOGICAL TRAITS IN CLARKIA DUDLEYANA. II. CONSTANCY OF WITHIN-POPULATION GENETIC VARIANCE

Recent quantitative genetic studies have attempted to infer long-term selection responsible for differences in observed phenotypes. These analyses are greatly simplified by the assumption that the within-population genetic variance remains constant through time and over space, or for the multivariate case, that the matrix of additive genetic variances and covariances (G matrix) is constant. We examined differences in G matrices and the association of these differences with differences in multivariate means (Mahalanobis D²) among 11 populations of the California endemic annual plant, Clarkia dudleyana. Based on nine continuous morphological traits, the relationship between Mahalanobis D² and a distance measure summarizing differences in G matrices reflected no concomitant change in (co)variances with changes in means. Based on both broad- and narrow-sense analyses, we found little evidence that G matrices differed between populations. These results suggest that both the additive and nonadditive (co)variances for traits have remained relatively constant despite changes in means.     

HOW SIMILAR ARE GENETIC CORRELATION STRUCTURES? DATA FROM MICE AND RATS

An integral assumption of many models of morphometric evolution is the equality of the genetic variance-covariance structure across evolutionary time. To examine this assumption, the quantitative-genetic aspects of morphometric form are examined for eight pelvic traits in laboratory rats (Rattus norvegicus) and random-bred ICR mice (Mus musculus). In both species, all traits are significantly heritable, and there are significant phenotypic and genetic correlations among traits, although environmental correlations among the eight traits are low. The size relations among the pelvic variables are isometric. Three matrix-permutation tests are used to examine similarity of phenotypic, genetic, and environmental covariance and correlation matrices within and between species. Independent patterns of morphometric covariation and correlation arise from genetic and environmental effects within each species and from environmental effects between species. The patterns of phenotypic and genetic covariation and correlation are similar within each species, and the phenotypic and genetic correlations are also similar between these species. However, genetic covariance matrices show no significant statistical association between species. It is suggested that the assumption of equality of genetic variance-covariance structures across divergent taxa should be approached with caution.     

Contrasting responses of Peromyscus mice of Yosemite National Park to recent climate change

Accurately predicting the response of species to climate change is crucial for the preservation of contemporary species diversity. In the current study, we analyze the response of two congeneric small mammal species (Peromyscus maniculatus and Peromyscus truei) to recent climate change in the region of Yosemite National Park (California, USA). The generalist P. maniculatus did not change its distribution in response to climate change while the specialist P. truei substantially changed its geographic and elevational distribution in the region, expanding into Yosemite. Using molecular genetic techniques we found that a cryptic geographic shift in genetic variation may have occurred within the geographically stable P. maniculatus distribution. Using a combination of morphometric and molecular genetic techniques we confirmed that a P. truei subspecies previously identified as a habitat specialist expanded into new habitat types, suggesting that this subspecies is not in fact a habitat specialist. Instead, we propose that the range of this subspecies is instead limited by climatic variables currently varying in response to contemporary climate change. These results underscore the importance of verifying the natural‐history‐based assumptions used to develop predictive models of species' response to climate change.     

Investigating niche and lineage diversification in widely distributed taxa: phylogeography and ecological niche modeling of the Peromyscus maniculatus species group

The relationship between lineage formation and variation in the ecological niche is a fundamental evolutionary question. Two prevailing hypotheses reflect this relationship: niche conservatism and niche divergence. Niche conservatism predicts a pattern where sister taxa will occupy similar niche spaces; whereas niche divergence predicts that sister taxa will occupy different niche spaces. Widely distributed species often show distinct phylogeographic structure, but little research has been conducted on how the environment may be related to these phylogenetic patterns. We investigated the relationship between lineage divergence and environmental space for the closely related species Peromyscus maniculatus and P. polionotus utilizing phylogenetic techniques and ecological niche modeling (ENM). We estimated the phylogenetic relationship among individuals based on complete cytochrome b sequences that represent individuals from a majority of the species ranges. Niche spaces that lineages occupy were estimated by using 12 environmental layers. Differences in niche space were tested using multivariate statistics based on location data, and ENMs were employed using maximum entropy algorithms. Two similarity indices estimated significant divergence in environmental space based on the ENM. Six geographically structured lineages were identified within P. maniculatus. Nested within P. maniculatus we found that P. polionotus recently diverged from a clade occupying central and western United States. We estimated that the majority of the genetic lineages occupy distinct environmental niches, which supports a pattern of niche divergence. Two sister taxa showed niche divergence and represent different ecomorphs, suggesting morphological, genetic and ecological divergence between the two lineages. Two other sister taxa were observed in the same environmental space based on multivariate statistics, suggesting niche conservatism. Overall our results indicate that a widely distributed species may exhibit both niche conservatism and niche divergence, and that most lineages seem to occupy distinct environmental niches.     

THE COVARIANCE STRUCTURE OF LIFE-HISTORY CHARACTERS IN DAPHNIA PULEX

The genetic covariance structure for life-history characters in two populations of cyclically parthenogenetic Daphnia pulex indicates considerable positive correlation among important fitness components, apparently at odds with the expectation if antagonistic pleiotropy is the dominant cause of the maintanence of genetic variation. Although there is no genetic correlation between offspring size and offspring number, present growth and present reproduction are both strongly positively correlated genetically with future reproduction, and early maturity is genetically correlated with larger clutch size. Although the ubiquity of antagonistic pleiotropy has been recently questioned, there are peculiarities of cyclical parthenogenesis that could lead to positive life-history covariance even when negative covariance would be expected in a similar sexual species. These include the influence of nonadditive gene action on evolution in clonally reproducing organisms, and the periodic release of hidden genetic variance within populations of cyclical parthenogens. Examination of matrix similarity, using the bootstrap for distribution-free hypothesis testing, reveals no evidence to suggest that the genetic covariance matrices differ between the populations. However, there is considerable evidence that the phenotypic and environmental covariance matrices differ between populations. These results indicate approximate stability of the genetic covariance matrix within species, an important assumption of many phenotypic evolution models, but should caution against the use of phenotypic in place of genetic covariance matrices.     

VARIATION IN GENETIC ARCHITECTURE OF CALLING SONG AMONG POPULATIONS OF ALLONEMOBIUS SOCIUS,A. FASCIATUS,AND A HYBRID POPULATION: DRIFT OR SELECTION?

Predictions using quantitative genetic models generally assume that the variance-covariance matrices remain constant over time. This assumption is based on the supposition that selection is generally weak and hence variation lost through selection can be replaced by new mutations. Whether this is generally true can only be ascertained from empirical studies. Ideally for such a study we should be able to make a prediction concerning the relative strength of selection versus genetic drift. If the latter force is prevalent then the variance-covariances matrices should be proportional to each other. Previous studies have indicated that females in the two sibling cricket species Allonemobius socius and A. fasciatus do not discriminate between males of the two species by their calling song. Therefore, differences between the calling song of the two males most likely result from drift rather than sexual selection. We test this hypothesis by comparing the genetic architecture of calling song of three populations of A. fasciatus with two populations of A. socius. We found no differences among populations within species, but significant differences in the G (genetic) and P (phenotypic) matrices between species, with the matrices being proportional as predicted under the hypothesis of genetic drift. Because of the proportional change in the (co)variances no differences between species are evident in the heritabilities or genetic correlations. Comparison of the two species with a hybrid population from a zone of overlap showed highly significant nonproportional variation in genetic architecture. This variation is consistent with a general mixture of two separate genomes or selection. Qualitative conclusions reached using the phenotypic matrices are the same as those reached using the genetic matrices supporting the hypothesis that the former may be used as surrogate measures of the latter.     

Nonlinear selection and the evolution of variances and covariances for continuous characters in an anole

The pattern of genetic variances and covariances among characters, summarized in the additive genetic variance‐covariance matrix, G , determines how a population will respond to linear natural selection. However, G itself also evolves in response to selection. In particular, we expect that, over time, G will evolve correspondence with the pattern of multivariate nonlinear natural selection. In this study, we substitute the phenotypic variance‐covariance matrix ( P ) for G to determine if the pattern of multivariate nonlinear selection in a natural population of Anolis cristatellus, an arboreal lizard from Puerto Rico, has influenced the evolution of genetic variances and covariances in this species. Although results varied among our estimates of P and fitness, and among our analytic techniques, we find significant evidence for congruence between nonlinear selection and P , suggesting that natural selection may have influenced the evolution of genetic constraint in this species.     

RESISTANCE OF GENETIC CORRELATION STRUCTURE TO DIRECTIONAL SELECTION IN DROSOPHILA MELANOGASTER

The genetic covariance and correlation matrices for five morphological traits were estimated from four populations of fruit flies, Drosophila melanogaster, to measure the extent of change in genetic covariances as a result of directional selection. Two of the populations were derived from lines that had undergone selection for large or small thorax length over the preceding 23 generations. A third population was constituted using flies from control lines that were maintained with equivalent population sizes as the selected lines. The fourth population contained flies from the original cage population from which the selected and control lines had been started. Tests of the homogeneity of covariance matrices using maximum likelihood techniques revealed significant changes in covariance structure among the selected lines. Prediction of base population trait means from selected line means under the assumption of constant genetic covariances indicated that genetic covariances for the small population differed more from the base population than did the covariances for the large population. The predicted small population means diverged farther from the expected means because the additive genetic variance associated with several traits increased in value and most of the genetic covariances associated with one trait changed in sign. These results illustrate that genetic covariances may remain nearly constant in some situations while changing markedly in others. Possible developmental reasons for the genetic changes are discussed.     

Differences in daily torpor patterns among three southeastern species ofPeromyscus

Summary Three subspecies ofPeromyscus inhabiting the montane, foothill, and coastal plain regions of the Carolinas were trapped in midwinter and the occurrence of spontaneous and ration-induced daily torpor was monitored via biotelemetric determination of body temperature. All tests were undertaken with field-caught mice that were subjected to a minimum of laboratory acclimation (two days). The tendency to enter torpor in the presence of adequate food was highest inP. maniculatus nubiterrae, whose natural montane habitat presents it with the greatest seasonal stress in terms of ambient temperature and food availability. This species exhibited significantly (P<0.05) longer spontaneous torpor bouts than did the two lowland subspecies,P. gossypinus gossypinus andP. leucopus leucopus (Table 1). Restriction of food to one-half thead libitum level increased the frequency, duration, and depth (mean minimum body temperature) of torpor in all three species (Fig. 1).P. maniculatus, however, displayed significantly (P<0.001) longer episodes of torpor induced by rationing than did either of the other two subspecies. The ability to compensate for a reduction in energy intake by adjusting levels of energy utilization may profoundly affect survival during short-term environmental stress in any of these three species.     

Comparative paternal and infanticidal behavior of sympatric white-footed mice (Peromyscus leucopus noveboracensis) and deermice (P. maniculatus nubiterrae)

We studied parental and infanticidal behavior in the field andlaboratory in two ecologically equivalent and sympatric congeners,white-footed mice, Peromyscus leucopus noveboracensis, and deermice,P. maniculatus nubiterrae. Despite their close phylogeneticrelationship and ecological similarity, various aspects of parentaland nesting behavior of the two species were significantly different.P. maniculatus males were more paternal than were P. leucopusmales in that they retrieved pups, nested with pregnant femalesand females with newborn pups, and formed longer associationswith females than did P. leucopus males. Thus, P. m. nubiterraeexhibited more pair-bonding (monogamous) characteristics thandid either P. leucopus or P. m. bairdi, as reported in otherstudies. The behavioral differences may represent the differentevolutionary history of the three subspecies. Infanticidal behavior,however, was similar in both species. Dispersing and unmatedmales killed strange pups placed in experimental test chambersin the field, whereas mated males did not kill pups within theirown home ranges. Resident females of both species were moreinfanticidal than were males, killing pups in 90% of the trials.The results support the sexual selection and resource competitionhypotheses for male and female infanticide, respectively. [BehavEcol 1991; 2: 38-45]     

Population divergence of genetic (co)variance matrices in a subdivided plant species,Brassica cretica

Abstract The present study of Brassica cretica had two objectives. First, we compared estimates of population structure (Q_st) for seven phenotypic characters with the corresponding measures for allozyme markers (F_st) to evaluate the supposition that genetic drift is a major determinant of the evolutionary history of this species. Secondly, we compared the genetic (co)variance ( G ) matrices of five populations to examine whether a long history of population isolation is associated with large, consistent differences in the genetic (co)variance structure. Differences between estimates of F_st and Q_st were too small to be declared significant, indicating that stochastic processes have played a major role in the structuring of quantitative variation in this species. Comparison of populations using the common principal component (CPC) method rejected the hypothesis that the G matrices differed by a simple constant of proportionality: most of the variation involved principal component structure rather than the eigenvalues. However, there was strong evidence for proportionality in comparisons using the method of percentage reduction in mean‐square error (MSE), at least when characters with unusually high (co)variance estimates were included in the analyses. Although the CPC and MSE methods provide different, but complementary, views of G matrix variation, we urge caution in the use of proportionality as an indicator of whether genetic drift is responsible for divergence in the G matrix.     

Experimental tests of nest site competition in two Peromyscus species

The importance of interspecific competition for nest sites between the white-footed mouse (Peromyscus leucopus noveboracensis) and the cloudland deermouse (P. maniculatus nubiterrae) were investigated in the montane forests of southwestern Virginia over 3 years. Trials were conducted for both species using large, outdoor enclosures in order to examine: (i) nest site preference in isolation and (ii) nest site selection made in the presence of potential competitors. Both species demonstrated a strong preference for arboreal nest sites when tested without competitors present. After the introduction of a heterospecific intruder, P. leucopus often shifted to a non-arboreal nest while P. maniculatus continued to use arboreal nests. Intruding P. maniculatus displaced resident P. leucopus from P. leucopus' preferred nest sites in all 3 years while intruding P. leucopus never displaced P. maniculatus. Neither species was routinely displaced in conspecific trials. Resident P. maniculatus also excluded P. leucopus from access to preferred nesting sites in all three years while P. leucopus were only able to exclude P. maniculatus in the 3rd year. Both species exhibite relatively low frequencies of exclusion in conspecific trials with the exception of P. maniculatus which excluded high proportions of conspecific intruders in the second year. We suggest that the asymmetrical advantage enjoyed by P. maniculatus in nest site selection may result from both site-specific effects and a species-specific influence on P. leucopus. Nonetheless, the intensity of such influence varied between years, perhaps as a function of population density, and did not appear to drastically influence continued coexistence of these congeners.     

The role of genetic constraints on the diversification of Iberian taxa of the genus Aquilegia (Ranunculaceae)

The microevolutionary process of adaptive phenotypic differentiation of quantitative traits between populations or closely‐related taxa depends on the response of populations to the action of natural selection. However, this response can be constrained by the structure of the matrix of additive genetic variance and covariance between traits in each population ( G matrix). In the present study, we obtained additive genetic variance and narrow sense heritability for 25 floral and vegetative traits of three subspecies of Aquilegia vulgaris, and one subspecies of Aquilegia pyrenaica through a common garden crossing experiment. For two vegetative and one floral trait, we also obtained the G matrix and genetic correlations between traits in each subspecies. The amount of genetic variation available in wild populations is not responsible for the larger differentiation of vegetative than floral traits found in this group of columbines. However, the low heritability of some traits constrained their evolution because phenotypic variability among taxa was larger for traits with larger heritability. We confirmed that the process of diversification of the studied taxa involved shifts in the G matrix, mainly determined by changes in the genetic covariance between floral and vegetative traits, probably caused by linkage disequilibrium in narrow endemic taxa. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 252–261.     

QUANTITATIVE GENETICS OF THE WING COLOR PATTERN IN THE BUCKEYE BUTTERFLY (PRECIS COENIA AND PRECIS EVARETE): EVIDENCE AGAINST THE CONSTANCY OF G

Models for the evolution of continuously varying traits use heritabilities, genetic correlations, and the G -matrix to quantify the genetic variation upon which selection acts. Given estimates of these parameters, it is possible to predict the long-term effects of selection, infer past selective forces responsible for observed differences between populations or species, and distinguish the effects of drift from selection. Application of these methods, however, requires the unproven assumption that the G -matrix remains constant from one generation to the next. This study examines the assumption of constancy for the wing pattern characteristics of two sibling species of butterflies, Precis coenia and P. evarete (Lepidoptera: Nymphalidae). Quantitative genetic parameters were estimated from parent-offspring regression. Two approaches were taken to test the null hypothesis of equality between species. First, pairwise tests between corresponding elements of G and between heritabilities and genetic correlations for the two species were constructed. Second, a modification of Bartlett's modified likelihood-ratio test was used to test for equality between the G -matrices. The matrix test failed to detect any between species differences. In contrast, pairwise comparision revealed significant differences. Thus, it appears that constancy cannot be assumed at the species level in quantitative genetic studies. In particular, the assumption of constancy was violated for the trait with the greatest difference in mean phenotype.     

Genetic diversity among African great apes based on mitochondrial DNA sequences

The mitochondrial DNA D-Loop region was sequenced, analyzed and used as a molecular marker for populations of chimpanzee (Pan troglodytes), bonobo (P. paniscus) and gorilla (Gorilla gorilla and G. beringei), and also compared with data previously reported for these taxa. In Gorilla, a main disjunction between western (G. gorilla) and eastern (G. beringei, including G. b. graueri) species was observed, as well as high mitochondrial diversity within the western species. The genetic distance values within G. gorilla (0.14) were higher than those between subspecies (eastern lowland and mountain 0.12). Likewise, values of genetic diversity within this species (0.05) were higher than those between species (western and eastern lowland gorilla 0.04). Similarly, in genus Pan a main differentiation between western (P. t. verus) and central forms (P. t. troglodytes and P. t. schweinfurthii) was observed. The obtained values of genetic distance and genetic diversity revealed that the central subspecies are closer to each other than either of them is to the western one, while bonobos composed a distinct clade that expresses a well-defined specific identity. The current distribution, phylogeny and levels of genetic diversity in African great ape populations are consistent with the hypothesis that Pleistocene climatic events led to cyclical periods of isolation in forest refugia followed by expansion and dispersal. The implications of this high level of genetic diversity for taxonomic classification, wildlife management and conservation are discussed.     

Variation in the genetic structure of Peromyscus populations. I. Genetic heterozygosity—its relationship to adaptive divergence

The genetic structure of nine Peromyscus maniculatus nebrascensis demes from southeastern Wyoming was determined by analyzing allozymes encoded by 23 genetic loci with polyacrylamide gel electrophoresis. Genetic variability is extremely high for two genetic parameters; the proportion of loci heterozygous per individual averaged 0.16, and the proportion of loci polymorphic per deme averaged 0.41. Previous estimates of genetic heterozygosity for species within the genus Peromyscus have a mean of 0.06. The results of the present study suggest that genetic heterozygosity is considerably higher within P. maniculatus demes than within demes of other species in the genus. Geographic range is correlated with heterozygosity among Peromyscus species, as is adaptive divergence into broad-niched species. These correlates suggest that high heterozygosity may reflect an adaptation to a variable environment.     

Genetics of Hemoglobin in the Deer Mouse, PEROMYSCUS MANICULATUS . II. Multiple Alleles at Regulatory Loci

Deer mice are polymorphic for electrophoretic hemoglobin phenotypes showing one, two, or three bands. Within the multibanded phenotypes, there is considerable variation in the hemoglobin partitioning, defined as the fraction of total hemoglobin made up by the secondary and tertiary bands. In subspecies sonoriensis, for example, hemoglobin partitionings range from 0.03 to 0.38. The inheritance of partitioning values is under remarkably strict genetic control. The genetic variation is additive and the narrow heritability is close to 1.0. The inheritance data can be modeled in precise detail by postulating multiple-allele polymorphisms at globin regulatory loci. Comparison of simulated versus actual inheritance data demonstrates that the so-called null structural alleles actually produce functional globins.—The genetic controls in Peromyscus may be analogous to those in primates. Unfortunately, the molecular mechanisms effecting the regulation are unknown. Different subspecies of P. maniculatus show strikingly different arrays of partitioning values, but the role of natural selection in maintaining the quantitative polymorphisms remains obscure.