RANDOM MATING IN THE NORTHERN FLICKER HYBRID ZONE: IMPLICATIONS FOR THE EVOLUTION OF BRIGHT AND CONTRASTING PLUMAGE PATTERNS IN BIRDS

The Red-shafted and Yellow-shafted Flickers hybridize in a narrow zone on the western Great Plains of North America. The two subspecies are markedly different in six plumage traits. Plumage phenotypes were scored for the male and female of 125 mated pairs from the hybrid zone. Correlation analyses revealed no tendency towards pairing of similar phenotypes. A binomial test was performed to determine whether flickers that have parental phenotypes and are presumably immigrants rather than hybrids tend to choose mates similar to themselves. This test again indicated random mating in the hybrid zone. These data complement earlier reports in providing an additional test of alternative hybrid zone theories. Random mating along with evidence of high reproductive success in hybrids suggests that reinforcement of premating reproductive isolation is not occurring and that speciation will not result from the dynamics of the hybrid zone. At least some of the plumage traits seem to be important in the integrated courtship and territorial behaviors of flickers. Since these plumage differences have no significance in mate choice, it is inferred that they evolved in an intrasexual selection context rather than in intersexual or species-recognition contexts. Selection gradients appear to be important in restricting hybridization to a narrow zone. The gradients could result from ecological selection or from sexual selection.     

A MODEL FOR THE EVOLUTION OF ASYMMETRICAL MALE HYBRID STERILITY AND ITS IMPLICATIONS FOR SPECIATION

Chromosomal analysis of several cases of asymmetrical male hybrid sterility in Drosophila has implicated the X- or the Y-chromosome and one or more autosomes. Here, I develop a model for the evolution of this phenomenon. An autosomal locus is assumed to affect viability and to interact with a Y-linked or an X-linked locus to determine male fertility. In a new environment, selection for viability favors a new allele at the autosomal locus, but incompatibility of this new allele with the sex-chromosome-linked gene generates male sterility. The incompatibility can be resolved if a new allele at the sex-linked locus invades the population. This results in nonreciprocal male hybrid sterility, the direction of the nonreciprocity being determined by the dominance or recessiveness of the new autosomal gene in its effect on fertility. It is shown that stable polymorphism for the autosomal locus is possible and that, if the equilibrium frequency of the new allele is above a critical value, the population will be constantly at the verge of speciation, “waiting” for the sex-linked mutation to occur. The appearance of this mutation causes a runaway process leading to rapid fixation of the new autosomal and sex-linked alleles. If the equilibrium frequency of the new autosomal allele is less than the critical value, deterministic speciation is impossible, but random drift may increase the frequency above the critical value and predispose the population to the invasion of the new sex-linked allele. Thus, both deterministic and stochastic modes of speciation are possible. Because deterministic speciation requires large selection coefficients, which impose a severe genetic load on the population, and because stochastic speciation requires repeated population bottlenecks, it is concluded that relative to the number of successful speciation events there will be many more events of deme extinction.     

CALIBRATING DIVERGENCE TIMES ON SPECIES TREES VERSUS GENE TREES: IMPLICATIONS FOR SPECIATION HISTORY OF APHELOCOMA JAYS

Estimates of the timing of divergence are central to testing the underlying causes of speciation. Relaxed molecular clocks and fossil calibration have improved these estimates; however, these advances are implemented in the context of gene trees, which can overestimate divergence times. Here we couple recent innovations for dating speciation events with the analytical power of species trees, where multilocus data are considered in a coalescent context. Divergence times are estimated in the bird genus Aphelocoma to test whether speciation in these jays coincided with mountain uplift or glacial cycles. Gene trees and species trees show general agreement that diversification began in the Miocene amid mountain uplift. However, dates from the multilocus species tree are more recent, occurring predominately in the Pleistocene, consistent with theory that divergence times can be significantly overestimated with gene‐tree based approaches that do not correct for genetic divergence that predates speciation. In addition to coalescent stochasticity, Haldane's rule could account for some differences in timing estimates between mitochondrial DNA and nuclear genes. By incorporating a fossil calibration applied to the species tree, in addition to the process of gene lineage coalescence, the present approach provides a more biologically realistic framework for dating speciation events, and hence for testing the links between diversification and specific biogeographic and geologic events.     

VARIABILITY IN TEMPERATURE AND HISTORICAL PATTERNS IN REPRODUCTION IN THE FUCUS DISTICHUS COMPLEX (HETEROKONTOPHYTA; PHAEOPHYCEAE): IMPLICATIONS FOR SPECIATION AND THE COLLECTION OF HERBARIUM SPECIMENS1

Natural and anthropogenic‐induced fluctuations in temperature can have profound effects on an organism's reproduction. The potential of herbarium collections for detecting changes in the timing of reproduction associated with interannual fluctuations in temperature from 1905 to 2003 was assessed in several taxa in the Fucus distichus (L.) emend. Powell complex from northern New England. Data were also used to evaluate whether air and/or sea temperature and North Atlantic Oscillation indices can cause overlap in the reproductive seasonalities of these taxa, a potential mechanism that prevents speciation. For all taxa, there was much variability in reproductive seasonalities among years. Discerning potential correlations with air or sea temperature was difficult because of a suspected bias to collect reproductive specimens at times when most of the population was nonreproductive. Nevertheless, there was a trend for seawater temperature to explain aseasonal reproduction for some taxa. Moreover, the existing archive (1895–2003) shows that the reproductive seasons of these taxa often overlap, and we suggest that interannual variability in temperature may often inhibit speciation. Suggestions also include archive of both reproductive and vegetative materials as well as coordinated sampling in critical biogeographic regions. No one investigator or institution can accomplish this, but phycological societies could organize and sustain such efforts.     

THE DISPERSAL BARRIER IN THE TROPICAL PACIFIC: IMPLICATIONS FOR MOLLUSCAN SPECIATION AND EXTINCTION

Stretches of deep ocean constitute barriers to the dispersal of many shallow-water marine species in the tropical Pacific. The purpose of this study was to assess the selectivity of these barriers with respect to the habitat characteristics, adult size, and predation-related shell architecture of gastropods, and to explore the implications of this selectivity for macroevolutionary patterns of extinction and speciation. The dispersal barrier between continental islands (represented in my collections by species from eastern Indonesia, the southern Philippines, and the north coast of New Guinea) and the nearby oceanic Palau Islands was studied by evaluating the percentage of each architectural and habitat category that is present on the continental islands but missing in Palau. The barrier is significantly more effective against sand-dwelling species than against rock-dwellers, and among rock-dwellers it is most effective against aperturally unarmored taxa. Barriers between Palau and Guam, Guam and the Hawaiian Islands, and the Line Islands and the tropical Eastern Pacific are generally unselective with respect to substratum type and architecture. The fact that narrow-apertured species are less affected by the barrier between the continental islands and Palau than are other rock-dwelling gastropods is consistent with the interpretation that this group has been unusually resistant to extinction and highly susceptible to founder speciation when oceanic circulation is altered. These patterns of susceptibility and geographical distribution may explain why armored gastropods have increased in numbers relative to unarmored ones in the tropical Pacific during the Cenozoic.     

AGE AND MOVEMENT OF A HYBRID ZONE: IMPLICATIONS FOR DISPERSAL DISTANCE IN POCKET GOPHERS AND THEIR CHEWING LICE

Historical flood records for the Rio Grande Valley of New Mexico suggest that a pocket gopher (Thomomys bottae) hybrid zone previously thought to be 10,000 years old may actually be closer to 50 years old. Measured zone width (defined genetically) is consistent with the hypothesis of recent contact, if we assume a reasonable dispersal distance of approximately 400 m/year for pocket gophers. A five-year study of movement of the contact zone between the two species of chewing lice that parasitize these pocket gophers also is consistent with the hypothesis of recent origin of the zone.     

FLICKER RESPONSE CONTOURS FOR THE SPARROW,AND THE THEORY OF THE AVIAN PECTEN

The flicker contour for the house sparrow Passer domesticus is duplex, corresponding to the presence of both rods and cones in the retina. The presence of the pecten brings about changes in the "cone" part of the contour when the light-time in the flash cycle is varied. These changes are of the same sort as those we have already described for the visually simplex zebra finch, and for man provided with an artificial "pecten shadow." The changes are such as to greatly enhance flicker acuity for small dark-times (moving stripe technique). The form of the scotopic part of the duplex contour (also as in the case with man) gives no evidence that rod excitation is specifically influenced by the presence of the pecten. The changing integration of "rod" and "cone" effects as the light-time fraction is altered provides another means of testing the theory used for the analytical separation of the two components of the duplex flicker contour.     

ADAPTIVE SIGNIFICANCE OF FLOWER COLOR AND INTER-TRAIT CORRELATIONS IN AN IPOMOPSIS HYBRID ZONE

Flower color is often viewed as a trait that signals rewards to pollinators, such that the relationship between flower color and plant fitness might result from its association with another trait. We used experimental manipulations of flower color and nectar reward to dissociate the natural character correlations present in a hybrid zone between Ipomopsis aggregata and Ipomopsis tenuituba. Isozyme markers were used to follow the male and female reproductive success of these engineered phenotypes. One field experiment compared fitnesses of I. aggregata plants that varied only in flower color. Plants with flowers painted red received more hummingbird visits and sired more seeds than did plants with flowers painted pink or white to match those of hybrids and I. tenuituba. Our second field experiment compared fitnesses of I. aggregata, I. tenuituba, and hybrid plants in an unmanipulated array and in a second array where all flowers were painted red. In the unmanipulated array, I. aggregata received more hummingbird visits, set more seeds per flower, and sired more seeds per flower. These fitness differences largely disappeared when the color differences were eliminated. The higher male fitness of I. aggregata was due to its very high success at siring seeds on conspecific recipients. On both I. tenuituba and hybrid recipients, hybrid plants sired the most seeds, despite showing lower pollen fertility than I. aggregata in mixed donor pollinations in the greenhouse. Ipomopsis tenuituba had a fitness of only 13% relative to I. aggregata when traits varied naturally, compared to a fitness of 36% for white relative to red flowers when other traits were held constant.     

HISTORICAL ALLOPATRY AND THE BIOGEOGRAPHY OF SPECIATION IN THE PROSOBRANCH SNAIL GENUS NUCELLA

Two recently diverged northeastern Pacific sibling snail species, Nucella ostrina and N. emarginata, currently inhabit adjacent zoogeographic provinces. Their distributions overlap in central California to the north of a major faunal boundary at Point Conception, California (PC). To test the hypothesis that modern sympatry is due to a recent northward range expansion by N. emarginata, I analyzed the population structures of both species with nuclear (allozyme) and mitochondrial DNA (mtDNA) markers. Populations of N. emarginata in the region of overlap exhibit significantly lower heterozygosity and allelic diversity than either populations to the south of PC or populations of N. ostrina. A single mtDNA haplotype characterizes all but one population of N. emarginata sampled in this region, but no haplotype to the south of PC is found at more than one locality. MtDNA haplotypes and allozyme allele frequencies also indicate monophyly of central California populations of N. emarginata. Sharp differences in allelic diversity over small geographic distances may reflect the action of natural selection, but because both nuclear and mtDNA markers display concordant patterns, a range expansion across PC best explains patterns of genetic variation in N. emarginata. Allozymes and mtDNA also reveal that the geologically older N. ostrina is paraphyletic with respect to N. emarginata. This pattern is consistent with, but not indicative of, a peripheral isolation model of speciation. Low genetic diversity is also expected if a significant bottleneck occurred at speciation. However, low allelic diversity is not universal throughout the geographic range of N. emarginata; high allelic diversity at the southern end of the distribution of N. emarginata suggests that in the past N. emarginata has been geographically restricted much further south than PC. A northward range expansion across PC by N. emarginata may thus represent only the most recent postglacial movement by the species. The thermal and oceanographic discontinuities found at PC may not have been directly involved in geographic isolation if N. emarginata originated much further south of this modern boundary. Despite uncertainty regarding the exact spatial distribution of populations at speciation, genetic data indicate that even though N. ostrina and N. emarginata currently exhibit a broad range of geographic overlap, speciation was likely allopatric and was initiated by physical isolation of populations in different zoogeographic provinces.     

CLINES FOR HYBRID DYSFUNCTION IN A GRASSHOPPER HYBRID ZONE

Two subspecies of the grasshopper Chorthippus parallelus meet in the Pyrenees forming a hybrid zone several kilometers wide. Crosses between the two pure taxa result in sterile male offspring and normal females (i.e., Haldane's rule applies). However, no such dysfunction has been detected in hybrid males collected through the center of the hybrid zone. By assessing the level of dysfunction in the offspring of reciprocal crosses, it was possible to map clines for the genes responsible for dysfunction through the zone. This analysis shows that there is no abrupt transition between incompatible genomes in the field. Crosses were also made between females collected from a transect spanning the hybrid zone and pure males of both subspecies. This reveals noncoincident clines for dysfunction near the center of the hybrid zone such that the dysfunction expressed in the offspring of these crosses is less than expected from simple models. More complex models involving interaction among genes must be invoked. Also, the possibility exists that since the postglacial contact of these two grasshopper taxa, hybrid dysfunction has become ameliorated by the evolution of modifiers. This hybrid zone is thought to be a tension zone, maintained by a balance between selection against hybrid genotypes and dispersal into the zone center. The lessening of hybrid disadvantage over time through the breakdown of epistatic interactions by recombination or through modification could account for the general lack of dysfunction in field collected hybrids today.     

EVOLUTIONARY IMPLICATIONS OF DIVERGENT CLINES IN AN AVIAN (MANACUS: AVES) HYBRID ZONE

Abstract A previous study of the hybrid zone in western Panama between white‐collared (Manacus candei) and golden‐collared manakins (M. vitellinus) documented the unidirectional introgression of vitellinus male secondary sexual traits across the zone. Here, we examine the hybrid zone in greater genetic and morphological detail. Statistical comparisons of clines are performed using maximum‐likelihood and nonparametric bootstrap methods. Our results demonstrate that an array of six molecular and two morphometric markers agree in cline position and width. Clines for male collar and belly color are similar in width to the first eight clines, but are shifted in position by at least five cline widths. The result is that birds in intervening populations are genetically and morphometrically very like parental candei, but males have the plumage color of parental vitellinus. Neither neutral diffusion nor nonlinearity of color scales appear to be viable explanations for the large cline shifts. Genetic dominance of vitellinus plumage traits is another potential explanation that will require breeding experiments to test. Sexual selection remains a plausible explanation for the observed introgression of vitellinus color traits in these highly dimorphic, polygynous, lek‐mating birds. Two other clines, including a nondiagnostic isozyme locus, are similar in position to the main cluster of clines, but are broader in width. Thus, introgression at some loci is greater than that detected with diagnostic markers. Assuming that narrow clines are maintained by selection, variation in cline width indicates that selection is not uniform throughout the genome and that diagnostic markers are under more intense selective pressure. The traditional focus on diagnostic markers in studies of hybrid zones may therefore lead to underestimates of average introgression. This effect may be more pronounced in organisms with low levels of genetic divergence between hybridizing taxa.     

HYBRIDIZATION STUDIES ON THE HOST RACES OF EUROSTA SOLIDAGINIS: IMPLICATIONS FOR SYMPATRIC SPECIATION

We studied the inheritance of survival ability in host-associated populations of the tephritid fly, Eurosta solidaginis, to test predictions of sympatric speciation models. Eurosta solidaginis induces galls on two species of goldenrod, Solidago altissima and S. gigantea. The host-associated populations have been hypothesized to be host races that originated in sympatry (Craig et al. 1993). We found evidence for disruptive selection for host use, which is a critical assumption of sympatric speciation models. Each host race had higher survival rates on their host plant than on the alternative host. F₁ and backcross hybrids also had lower survival rates than the pure host-race flies on their host plant. Since assortative mating occurs due to host-plant preference (Craig et al. 1993) this would select for divergence in host preference. Low hybrid survival could have been due to strong genetic incompatibilities of the populations or due to host adaptation by each population. Strong genetic incompatibilities would result in poor survival on all host plants, while host adaptation could result in low overall survival with high hybrid survival on some host plants with particularly “benign” environments. High survival of F₁, F₂, and backcross hybrids on some plant genotypes in some years supported the host adaptation hypothesis. F₁ flies mated and oviposited normally and produced viable F₂ and backcross hybrids indicating gene flow is possible between the host races. A few flies developed and emerged on the alternative host plant. This demonstrates that genes necessary to utilize the alternative host exist in both host races. This could have facilitated the origin of one of the populations via a host shift from the ancestral host. The inheritance of survival ability appears to be an autosomal trait. We did not find evidence that survival ability was maternally influenced or sex linked.     

PATTERNS OF HYBRIDIZATION IN THE PIRIQUETA CAROLINIANA COMPLEX IN CENTRAL FLORIDA: EVIDENCE FOR AN EXPANDING HYBRID ZONE

We have identified a broad zone of hybridization between two morphologically and ecologically distinct herbaceous perennial taxa (morphotypes) within the Piriqueta caroliniana complex, which extends more than 300 km across the central Florida peninsula. Phylogeographic analyses indicate that the caroliniana morphotype has been present in north and central Florida since the early Pleistocene and that the viridis morphotype has immigrated into southern Florida much more recently. We examine the distribution of diagnostic morphological characters and nuclear genetic markers to assess the extent and patterns of introgression in this system. The results are consistent with the hypothesis that this hybrid zone has expanded north in recent history as viridis alleles have introgressed into regions that were previously occupied by populations of caroliniana. Genetic markers diagnostic for caroliniana have consistently high frequencies across the hybrid zone, whereas markers for viridis are extremely variable among populations with frequency reversals in adjacent populations. The latter pattern is probably the result of the combined stochastic effects of dispersal and drift on viridis alleles as they introgressed northward. Additional evidence for the recent expansion of this hybrid zone comes from patterns of variation for morphological and genetic markers. As expected for an expanding hybrid zone, within-population morphological variation was greatest toward the advancing front of introgression and levels of genetic variation for neutral diagnostic markers were greatest in the region of initial contact and lower in areas of recent expansion. The observed patterns of variation suggest that at least some hybrid genotypes have high fitnesses, which has led to the expansion of the hybrid zone via the displacement of parental genotypes in central Florida.     

INCIPIENT SPECIATION DESPITE LITTLE ASSORTATIVE MATING: THE YELLOW‐RUMPED WARBLER HYBRID ZONE

Hybrid zones between recently diverged taxa are natural laboratories for speciation research, allowing us to determine whether there is reproductive isolation between divergent forms and the causes of that isolation. We present a study of a classic avian hybrid zone in North America between two subspecies of the yellow‐rumped warbler (Dendroica coronata). Although previous work has shown very little differentiation in mitochondrial DNA across this hybrid zone, we identified two nuclear loci (one sex‐linked and one autosomal) that show fixed differences across the hybrid zone, in a close concordance with patterns of plumage variation. Temporal stability and limited width of the hybrid zone, along with substantial linkage disequilibrium between these two diagnostic markers in the center of the zone, indicate that there is moderate reproductive isolation between these populations, with an estimated strength of selection maintaining the zone of 18%. Pairing data indicate that assortative mating is either very weak or absent, suggesting that this reproductive isolation is largely due to postmating barriers. Thus, despite extensive hybridization the two forms are distinct evolutionary groups carrying genes for divergent adaptive peaks, and this situation appears relatively stable.     

ECOLOGICAL SPECIATION IN STICKLEBACKS: ENVIRONMENT-DEPENDENT HYBRID FITNESS

“Ecological” speciation occurs when reproductive isolation evolves as a consequence of divergent selection between populations exploiting different resources or environments. We tested this hypothesis of speciation in a young stickleback species pair by measuring the direct contribution of ecological selection pressures to hybrid fitness. The two species (limnetic and benthic) are strongly differentiated morphologically and ecologically, whereas hybrids are intermediate. Fitness of hybrids is high in the laboratory, especially F₁ and F₂ hybrids (backcrosses may show some breakdown). We transplanted F₁ hybrids to enclosures in the two main habitats in the wild to test whether the distribution of resources available in the environment generates a hybrid disadvantage not detectable in the laboratory. Hybrids grew more slowly than limnetics in the open water habitat and more slowly than benthics in the littoral zone. Growth of F₁ hybrids was inferior to the average of the parent species across both habitats, albeit not significantly. The contrast between laboratory and field results supports the hypothesis that mechanisms of F₁ hybrid fitness in the wild are primarily ecological and do not result from intrinsic genetic incompatibilities. Direct selection on hybrids contributes to the maintenance of sympatric stickleback species and may have played an important role in their origin.     

WAITING FOR SPECIATION: THE EFFECT OF POPULATION SUBDIVISION ON THE TIME TO SPECIATION

We study the time required for speciation in a species that is divided into small versus large populations. Following Dobzhansky and Muller, we assume that hybrid sterility or inviability is caused by “complementary genes,” that is, by the accumulation of genes that cause sterility or inviability when brought together in hybrids but that have no deleterious effect on their normal species genetic background. When divergence between populations is caused by genetic drift, we show that the time to speciation is independent of population subdivision: speciation occurs just as quickly in a species split into a few large populations as into many small populations. When divergence is driven by natural selection, however, the time to speciation is very sensitive to population subdivision and speciation occurs most rapidly when a species is split into two large populations. These results contradict several popular intuitions about the effect of population size on speciation.     

THEORY AND MEASUREMENT OF VISUAL MECHANISMS : VIII. THE FORM OF THE FLICKER CONTOUR

Flicker response curves (man) obtained with images formed entirely within the fovea are like those secured with lower animals having only one general class of retinal receptors. They are normal probability integrals (F vs. log I_m), and the properties of their parameters agree with those for visually simplex animals and for the "cone" portions of contours exhibiting visual duplexity. By several different procedures, involving experimental modifications of the "cone" curve, the "rod" part of the typical human duplex curve can be obtained free from overlapping by the extrapolated "cone" curve. It then has the probability integral form which the lower segment does not directly exhibit when combined with "cone" effects. These results are discussed with reference to the statistical nature of the fundamental form of the flicker contour and to the interpretation of duplex curves produced by the neural integration of two independently modifiable groups of sensory effects.     

HABITAT PREFERENCE IN THE BOMBINA HYBRID ZONE IN CROATIA

This paper demonstrates the effect of habitat heterogeneity and a habitat preference on the genetic structure of a hybrid zone between the toads Bombina bombina and B. variegata (Anura: Discoglossidae); 1613 toads from 85 sites across a transect near Pe??enica, Croatia, were scored for five unlinked diagnostic allozyme markers. These were found to be largely concordant. Aside from minor systematic deviations, there was little variance in allele frequency among loci within sites. Yet the allele frequencies did not follow a smooth cline, but formed a mosaic in the center, such that neighboring sites could differ markedly in their enzyme score. A detailed ecological survey revealed a correlation between this pattern and habitat. In keeping with the typical breeding sites of the parental taxa, B. bombina-like hybrids were found more often in ponds, whereas B. variegata-like hybrids were more common in puddles. In addition, there was significant heterozygote deficit (F_IS) and strong linkage disequilibrium (R), both of which were stronger on the B. bombina side of the transect, and stronger in puddles than ponds. Mark-recapture data showed: (1) that the animals disperse beyond the scale of the habitat pattern; (2) frequent turn-over of individuals within sites; and (3) nonrandom movement between two sites of different habitat type. We conclude that an active habitat preference must contribute to the observed association between marker alleles and habitat. As a consequence, there is incomplete mixing of the two gene pools, which could explain the high level of F_IS and R. The asymmetry in these parameters may reflect asymmetry in the preference or in the distribution of habitats across the zone. We discuss the implications of habitat preference for the dynamics of hybrid zones.     

AN EVALUATION OF THE HYBRID SPECIATION HYPOTHESIS FOR XIPHOPHORUS CLEMENCIAE BASED ON WHOLE GENOME SEQUENCES

Once thought rare in animal taxa, hybridization has been increasingly recognized as an important and common force in animal evolution. In the past decade, a number of studies have suggested that hybridization has driven speciation in some animal groups. We investigate the signature of hybridization in the genome of a putative hybrid species, Xiphophorus clemenciae, through whole genome sequencing of this species and its hypothesized progenitors. Based on analysis of this data, we find that X. clemenciae is unlikely to have been derived from admixture between its proposed parental species. However, we find significant evidence for recent gene flow between Xiphophorus species. Although we detect genetic exchange in two pairs of species analyzed, the proportion of genomic regions that can be attributed to hybrid origin is small, suggesting that strong behavioral premating isolation prevents frequent hybridization in Xiphophorus. The direction of gene flow between species is potentially consistent with a role for sexual selection in mediating hybridization.