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Estimates of selection and gene flow from measures of cline width and linkage disequilibrium in heliconius hybrid zones.

Hybrid zones can yield estimates of natural selection and gene flow. The width of a cline in gene frequency is approximately proportional to gene flow (sigma) divided by the square root of per-locus selection (square root of s). Gene flow also causes gametic correlations (linkage disequilibria) between genes that differ across hybrid zones. Correlations are stronger when the hybrid zone is narrow, and rise to a maximum roughly equal to s. Thus cline width and gametic correlations combine to give estimates of gene flow and selection. These indirect measures of sigma and s are especially useful because they can be made from collections, and require no field experiments. The method was applied to hybrid zones between color pattern races in a pair of Peruvian Heliconius butterfly species. The species are Müllerian mimics of one another, and both show the same changes in warning color pattern across their respective hybrid zones. The expectations of cline width and gametic correlation were generated using simulations of clines stabilized by strong frequency-dependent selection. In the hybrid zone in Heliconius erato, clines at three major color pattern loci were between 8.5 and 10.2 km wide, and the pairwise gametic correlations peaked at R approximately 0.35. These measures suggest that s approximately 0.23 per locus, and that sigma approximately 2.6 km. In erato, the shapes of the clines agreed with that expected on the basis of dominance. Heliconius melpomene has a nearly coincident hybrid zone. In this species, cline widths at four major color pattern loci varied between 11.7 and 13.4 km. Pairwise gametic correlations peaked near R approximately 1.00 for tightly linked genes, and at R approximately 0.40 for unlinked genes, giving s approximately 0.25 per locus and sigma approximately 3.7 km. In melpomene, cline shapes did not perfectly fit theoretical shapes based on dominance; this deviation might be explained by long-distance migration and/or strong epistasis. Compared with erato, sample sizes in melpomene are lower and the genetics of its color patterns are less well understood. In spite of these problems, selection and gene flow are clearly of the same order of magnitude in the two species. The relatively high per locus selection coefficients agree with "major gene" theories for the evolution of Müllerian mimicry, but the genetic architecture of the color patterns does not. These results show that the genetics and evolution of mimicry are still only sketchily understood.

Animals

Observations on the extent and temporal stability of latitudinal clines for alcohol dehydrogenase allozymes and four chromosome inversions in Drosophila melanogaster.

Previously we have presented evidence of large-scale latitudinal clines in the frequencies of four chromosome inversions and alleles at six enzyme loci in populations of D. melanogaster in Australasia, Asia and North America. Subsequent sampling by others in Japan and western U.S.A. has failed to repeat this observation for the steepest of the clines (alcohol dehydrogenase and the four chromosome inversions). We argue that this failure reflects the few populations and small latitudinal range sampled in these later studies. From extensive sampling over a long latitudinal transect in Australasia we here document Adh and inversion clines which are virtually identical to those originally obtained in different Australian populations four years earlier. We also repeat our observation that the Adh cline is largely independent of the cline in the linked inversion In(2L)t. We therefore retain our original conclusion that these polymorphisms are subject to natural selection. However the new Australasian data do not indicate an association between Adh and maximum rainfall which had been evident in the earlier data for Australasia, Asia and North America. We therefore retract our claim that the selective agent on Adh is related to rainfall.

Alcohol Dehydrogenase

Evidence for a link between local and seasonal cycles in gene frequencies and latitudinal gene clines in a cyclic parthenogen.

In an earlier study (Rhombergh et al., Can. J. Genet. Cytol. 27: 224-232, 1985) of natural populations of the cyclic parthenogenetic Rose aphids, Macrosiphum rosae, 6 out of 31 loci were found to be polymorphic and one locus (Esterase-4) showed cyclic seasonal changes in gene and genotypic frequencies. Assuming that the Est-4 polymorphism was balanced and due to some climatic factor that varies seasonally, and realizing that most environmental factors that vary seasonally also vary latitudinally, we predicted existence of a latitudinal gene cline at this locus. In the present study we surveyed four polymorphic loci (chosen to be used as markers) in six geographic populations spanning over 1200 km between the United States and Canada and found all four loci to have latitudinal clines. We think that the gene clines are due to a latitudinal cline in the degree of advancement of local populations through the seasonal cycle, and have called such a pattern a 'seasonal phase cline'. The results are discussed in relation to the temporal instability of local patterns and persistence of genetic variability on the large scale in aphids. It is argued that population structure of aphids makes retention of selectively neutral or weakly selected polymorphisms difficult.

Animals

Inference from clines stabilized by frequency-dependent selection.

Frequency-dependent selection against rare forms can maintain clines. For weak selection, s, in simple linear models of frequency-dependence, single locus clines are stabilized with a maximum slope of between square root of s/square root of 8 sigma and square root of s/square root of 12 delta, where sigma is the dispersal distance. These clines are similar to those maintained by heterozygote disadvantage. Using computer simulations, the weak-selection analytical results are extended to higher selection pressures with up to three unlinked genes. Graphs are used to display the effect of selection, migration, dominance, and number of loci on cline widths, speeds of cline movements, two-way gametic correlations ("linkage disequilibria"), and heterozygote deficits. The effects of changing the order of reproduction, migration, and selection, are also briefly explored. Epistasis can also maintain tension zones. We show that epistatic selection is similar in its effects to frequency-dependent selection, except that the disequilibria produced in the zone will be higher for a given level of selection. If selection consists of a mixture of frequency-dependence and epistasis, as is likely in nature, the error made in estimating selection is usually less than twofold. From the graphs, selection and migration can be estimated using knowledge of the dominance and number of genes, of gene frequencies and of gametic correlations from a hybrid zone.

Computer Simulation

Conditions for the existence of clines.

A very general partial differential equation in space and time satisfied by the gene frequency in a monoecious population distributed continuously over an arbitrary habitat is derived. The treatment is restricted to a single diallelic locus in the absence of mutation and random drift, and it is supposed that time is continuous, births and deaths occur at random, and migration is independent of genotype. With the further assumptions that migration is isotropic and homogeneous, the population density is constant and uniform (as permitted by the population regulation mechanism included in the formulation), and Hardy-Weinberg proportions obtain locally, this partial differential equation reduces to the simplest multidimensional generalization of the classical Fisher-Haldane cline model. The efficacy of migration and selection in maintaining genetic variability at equilibrium in this model is investigated by deducing conditions for the existence of clines under various circumstances. The effects of the degree of dominance, a neutral belt between the regions where a particular allele is advantageous and deleterious, finiteness of the habitat, and habitat dimensionality are evaluated. Provided at least one of the alleles is favored only in a finite region, excluding the special case in which its total effective selective coefficient is zero, if conditions for supporting a cline are too unfavorable because migration is too strong, selection is too weak, or both, a cline cannot exist at all. Thus, unless there is overdominance, the population must be monomorphic. It is possible for a cline which can barely exist under the prevailing ecological circumstances to show a large amount of variation in gene frequency.

Alleles

A hybrid zone comprising staggered chromosomal clines in the house mouse (Mus musculus domesticus).

In the vicinity of John o'Groats (Caithness, Scotland) there is a small karyotypic race of the house mouse (Mus musculus domesticus) characterized by a diploid number of 32 chromosomes, including the metacentrics 4.10, 9.12, 6.13 and 11.14. This race forms a hybrid zone with the standard British race (fully acrocentric chromosomes, 2n = 40). Although hybrid zones normally consist of several (or many) narrow character clines at the same position, this zone is unusual in that the chromosomal clines do not coincide. The cline for arm combination 11.14 is staggered relative to the 6.13 cline and both are separate from the clines for 4.10 and 9.12 (which may or may not coincide). A variety of explanations for the structure of the hybrid zone are discussed. It is possible that this may be a case of 'zonal raciation'.

Animals

The amplitude of circadian oscillations: temperature dependence, latitudinal clines, and the photoperiodic time measurement.

This paper develops several propositions concerning the lability of the amplitude of Drosophila circadian pacemakers. The first is that the amplitude of the pacemaker's motion, unlike its period, is markedly temperature-dependent. The second is that latitudinal variation in pacemaker amplitude (higher in the north) is responsible for two very different sets of observations on Drosophila circadian systems at successively higher latitudes. One of these is a cline in D. auraria's phase-shifting response to light, which steadily weakens in a succession of more northerly strains. The other, concerning D. littoralis in the very far north, is a cline in the rate at which eclosion activity becomes arrhythmic (the circadian rhythm damps out) in constant darkness; damping is faster in the north. The third proposition concerns a plausible selection pressure for the cline in pacemaker amplitude that we propose underlies the two directly observed clines. Two points are emphasized: (1) The amplitude of the pacemaker's daily oscillation declines as the duration of the entraining light pulse (photoperiod) is increased; and (2) the duration of the daily photoperiods throughout the breeding season is steadily increased as one moves toward the poles. Selection for conservation of pacemaker amplitude (during the breeding season) would produce the latitudinal cline we propose. The fourth, and final proposition is that since the amplitude of the pacemaker's daily motion responds systematically to change in photoperiod, amplitude is clearly one way--and a temperature-dependent way--in which insect circadian systems may sense seasonal change. These propositions concerning the temperature and latitude dependence of pacemaker amplitude may be relevant to a wider array of circadian pacemakers than Drosophila.

Animals

Gene frequency clines at X-linked or haplodiploid loci.

The equations governing gene frequency clines at X-linked or haplodiploid loci are derived. Clines at X-linked loci will be identical to corresponding clines at autosomal loci only under three restrictive conditions (a) no dominance, (b) dispersal distance the same in each sex, (c) average effect of alleles same in each sex. If any of these conditions are not met then the males and females will have different gene frequencies. Clinal variation in colour morph frequency in the bumble bee Bombus melanopygusis analysed. It is concluded that a minimum selection intensity acting on the queens on the order of 1 per cent or less is sufficient to maintain the cline.

Animals

The P-M hybrid dysgenesis cline in Eastern Australian Drosophila melanogaster: discrete P, Q and M regions are nearly contiguous.

The dramatic latitudinal cline in P-M hybrid dysgenesis characteristics along the east coast of Australia is not smooth. Tests of recent collections of Drosophila melanogaster from the southeastern coast define the previously described cline as comprising three discrete, apparently contiguous regions of P, Q and M phenotypes, respectively. Northern populations from Cairns (16.9 degrees SLat) to Ourimbah (33.4 degrees SLat) are phenotypically P; populations from Wollongong (34.4 degrees SLat) to Eden (37.1 degrees SLat) are Q; and populations from Genoa (37.5 degrees SLat) to Cygnet (43.2 degrees SLat) are M. The decline in P activity from northern Queensland (55-60% gonadal dysgenesis (GD) in cross A) to mid-New South Wales (20-30% GD in cross A) is gradual; proceeding south, there then is a sharp drop to Q populations (less than 10% GD in crosses A and A*). This drop in P activity occurs in only 150 km, across the urban and suburban area of Sydney. Q populations are then found south to Eden, but Genoa, only about 50 km further southeast, is clearly M (48% GD in cross A*), as are two populations further south. The two discontinuities in the P-M cline do not correspond to obvious climatic differences along the coast, nor to obvious barriers to dispersal of D. melanogaster. The cline has apparently not moved between 1983 and 1985-1986.

Animals

Molecular analysis of the P-M gonadal dysgenesis cline in eastern Australian Drosophila melanogaster.

The latitudinal cline in P-M gonadal dysgenesis potential in eastern Australia has been shown to comprise three regions which are, from north to south respectively, P, Q, and M, with the P-to-Q and Q-to-M transitions occurring over relatively short distances. The P element complements of 30 lines from different regions of the cline were determined by molecular techniques. The total amount of P element-hybridizing DNA was high in all lines, and it did not correlate in any obvious way with the P-M phenotypes of individual lines. The number of potentially full-sized P elements per genome was high in lines from the P regions, but variable or low among lines from the Q and M regions, and thus declined overall from north to south. A particular P element deletion-derivative, the KP element, occurred in all the tested lines. The number of KP elements was low in lines from the P region, much higher in lines from the Q region, and highest among lines from the M region, thus forming a cline reciprocal to that of the full-sized P elements. Another transposable element, hobo, which has been described as causing dysgenic traits similar to those of P-M hybrid dysgenesis, was shown to be present in all lines and to vary among them in number, but not in any latitudinal pattern. The P-M cline in gonadal dysgenesis potential can be inferred to be based on underlying clinal patterns of genomic P element complements. P activity of a line was positively correlated with the number of full-sized P elements in the line, and negatively correlated with the number of KP elements. Among Q and M lines, regulatory ability was not correlated with numbers of KP elements.

Animals

Genetic drift in clines which are maintained by migration and natural selection.

Genetic drift will cause a migration-selection cline to wobble about its expected position. A rough linear approximation is developed, valid when local populations are large. This is used to calculate effects of genetic drift on clines in a stepping-stone model with abrupt and with gradual changes of selection coefficients at a single haploid locus. Among the quantities calculated are measures of slope, standardized variation of gene frequencies around their expected values, and correlation among neighboring populations with respect to deviations from the expected gene frequencies. These quantities appear to be primarily functions of Ns and Nm for a given pattern of selection. Computer simulation gives rough confirmation of these results. Standardized variances of gene frequencies and correlation of neighbors differ along the cline in the case of smooth changes in selection. In no case is pathological behavior of gene frequency deviations found near the boundaries of selective regions. Local behavior of gene frequences of nearby colonies is approximately predicted by a simple adaptation of the stepping-stone theory of Kimura and Weiss. Approximate measures of the lateral variation of the midpoint of a cline and the probability of non-monotonicity are also calculated and discussed.

Gene Frequency

The genetic structure of a tribal population, the Yanomama Indians. XIV. Clines and their interpretation.

The Yanomama Indians are a South American tribe distributed over an irregular area approximately 200 X 300 miles. The gene frequencies observed at 12 loci in 47 villages within this area have been analyzed for the occurrence of clines. Apparently significant clines are observed for alleles of the Rh, MNSs, Kidd, Gm, Inv and serum albumin system. Available data concerning recent tribal expansion and admixture permit a tentative analysis of the causes of these clines. Although the action of selection cannot be rigorously excluded, it seems unlikely to be the major couse. Admixture with surrounding tribes plays a role which can be quantified because of the fortuitous cicumstance of two genetic markers for admixture. It is suggested that an important factor in the origin of these clines is the manner in which the tribe has recently expanded through successive village fissionings and a predominantly centrifugal pattern of village migration.

Alleles

New studies of the alcohol dehydrogenase cline in D. melanogaster from Mexico.

An altitudinal cline of frequencies of alcohol dehydrogenase alleles occurs in D. melanogaster populations of southeastern Mexico. A similar cline of two aldehyde oxidase alleles is present, but frequencies of esterase-6 alleles are not distributed clinically. Collections were made from small dispersed populations. Some gene flow occurred throughout the lowlands according to the distribution of two moderately endemic autosomal inversions and five previously described inversions. The clines are believed dependent on a limited gene flow between temperature races of D. melanogaster.

Alcohol Oxidoreductases

Clines in the colour polymorphism of Philaenus spumarius in Eastern Central Europe.

Populations of Philaemus spumarius (Homoptera) have been investigated in the Baltic States of the USSR, in Czechoslovakia and in Hungary. Colour morph frequencies in these highly polymorphic populations are compared with those reported earlier from northern Italy. Gradual changes in allele frequencies (clines) transect the study area, which lies in the most central part of the range of Philaenus in Europe. From north to south the allele pM increases, but pO decreases, in frequency. In their distribution, some of the other alleles also showed regional gradients. The possibility that visual selection varies regionally is dismissed on indirect grounds. Gradients in climatic severity, or in other environmental variables changing concomitantly with climate, are regarded as the primary cause of the observed clines and other differences between regions.

Alleles

Genetic drift in a cline.

A model is developed of genetic drift in a cline maintained by spatially varying natural selection and local dispersal of individuals. The model is analyzed by an approximation scheme which is valid for weak selection and small migration rates. The results, which are based on numerical iterations of the approximate equations, are that the cline is less steep than predicted on the basis of the deterministic theory but that for weak selection the correlation between random fluctuations in neighboring colonies is approximately the same as in models of migration and drift in the absence of selection.

Biological Evolution

Further evidence for latitudinal inversion clines in natural populations of Drosophila melanogaster from India.

Chromosomal analysis of eight Indian natural populations (six from north India and two from south India) of Drosophila melanogaster revealed the presence of 13 paracentric inversions, including one in the X chromosome. All four types of inversions--common cosmopolitan (4), rare cosmopolitan (3), recurrent endemic (2), and unique endemic (4)--were detected. The frequency of commonly occurring inversions and the level of inversion heterozygosity were found to be higher in the two southern populations. The south Indian populations are genetically more differentiated than those from the north. Also, latitudinal clines in the frequencies of the four common cosmopolitan inversions were detected. These results provide further evidence for the existence of inversion clines in Indian populations of D. melanogaster.

Animals

Latitudinal clines in the properties of a circadian pacemaker.

The circadian rhythm of eclosion activity and its pacemaker were analyzed in a series of latitudinal races of Drosophila auraria ranging from 34.2 degrees to 42.9 degrees N in Japan. The phase of the rhythm (psi EL) to the daily photoperiod (PP) changes as daylength is increased, and the slope of psi EL (PP) changes with latitude. Is is sufficiently greater in the north to cause a phase reversal of northern and southern races on long versus short photoperiods. This reversal is found in assays of the pacemaker's phase (psi PL) as well as that of the rhythm (psi EL). Assay of the pacemaker shows that its period (tau) is longer in northern than in southern races, and that the amplitude of its phase response curve (PRC) is lower in the north. The period of the rhythm in all latitudinal races is longer than 24 hr in short photoperiods (LD 1:23), but is probably less than 24 hr (as an aftereffect of photoperiod) in longer days such as LD 14:10. The observed north-south differences in the phase relation of both pacemaker and rhythm to the light cycle are explained by the latitudinal clines in pacemaker properties and a postulated aftereffect of photoperiod on tau. It is suggested that the latitudinal cline in PRC amplitude has functional significance in conserving the amplitude of the pacemaker's signal to the rest of the system it times. Computer simulation shows that without such a reduction in the perceived light intensity, pacemaker amplitude will be lowered by the increase in duration of the daily light at higher latitudes.

Animals

Convergence to spatial-temporal clines in the Fisher equation with time-periodic fitnesses.

The asymptotic behavior as t----infinity of the solutions with values in the interval (0, 1) of a reaction-diffusion equation of the form (Formula: see text) is studied. Conditions on m which are satisfied when m is nonincreasing in mu and which imply that every solution converges to some periodic limit function are found. Except in some very special and well-defined circumstances, the limit is the same for all solutions, so that it is a global attractor. This global attractor may be one of the trivial solutions 0 or 1, or it may be a spatial-temporal cline. The linear stability properties of the trivial states serve to distinguish between these cases.

Mathematics