Sympatric Races Research Articles

Host-driven phenotypic and phenological differentiation in sympatric races of a parasitic plant

Host specificity is a key factor influencing the ecology and evolutionary diversification of parasitic organisms. Host specialisation and geographic isolation are known to lead to the genetic differentiation of allopatric races in parasitic plants. However, how divergence can co-occur in sympatry remains largely unknown. We investigated phenological and phenotypic differentiation and potential reproductive isolation among three sympatric genetic races of Cytinus hypocistis (Cytinaceae) - an extreme endophytic holoparasite with a high degree of host specialisation. We compared spatio-temporal variations in flowering phenology, flower production, floral longevity, floral rewards, and morphology, and conducted inter-race pollinations among three races parasitising Cistus ladanifer, C. salviifolius, and Halimium halimifolium (Cistaceae) in six co-occurring populations. We found that host-defined genetic races differed significantly across multiple phenotypic and phenological aspects – a phenomenon previously overlooked due to the plants’ cryptic morphology. The race parasitising H. halimifolium showed earlier blooming, higher floral display, longer flowers, and higher pollen production and nectar concentration; the race on C. salviifolius showed later flowering, significantly lower floral display and smaller flowers with lower floral rewards; the race on C. ladanifer had intermediate characteristics. Genetic races were interfertile yet may remain differentiated by restricted gene flow and host-driven selection pressures. Together, our data point to a rare case of sympatric divergent evolution hiding in plain sight: apparently morphologically similar co-occurring parasite races can be genetically, phenotypically, and phenologically distinct. This hitherto unreported example of host-driven sympatric diversification challenges how species concepts are applied to cryptic parasitic plant races.

Ostrinia revisited: Evidence for sex linkage in European Corn Borer Ostrinia nubilalis (Hubner) pheromone reception

BackgroundThe European Corn Borer, Ostrinia nubilalis (Hubner), is a keystone model for studies on the evolution of sex pheromone diversity and its role in establishing reproductive isolation. This species consists of two sympatric races, each utilizing opposite isomers of the same compound as their major pheromone component. Female production and male response are congruent in each race, and males from each strain exhibit phenotypic differences in peripheral physiology. Both strains possess co-localized pheromone-sensitive olfactory sensory neurons characterized by a larger amplitude action potential (spike) responding to the major pheromone component, and a smaller spike amplitude cell responding to the minor component, i.e. the opposite isomer. These differences in amplitude correspond to differences in dendritic diameter between the two neurons. Previous studies showed that behavioral response to the pheromone blend was sex-linked, but spike amplitude response to pheromone components matched autosomal, not sex-linked inheritance.ResultsAs part of a larger study to finely map the loci responsible for pheromone communication in this species, we have reanalyzed peripheral physiology among parental, and first and second generation hybrids between the two pheromone strains using tungsten electrode electrophysiology. Our results reveal that differences in spike amplitude ratio between male pheromone-sensitive sensory neurons in O. nubilalis races are controlled, at least partially, by sex-linked genes that exhibit E-strain dominance.ConclusionsWe propose that peripheral olfactory response in O. nubilalis may be affected both by autosomal and sex-linked genes exhibiting a cross-locus dominance effect, and suggest that the genetic basis for pheromone reception and response in the species is more closely linked than previously thought.

The genetic structure of hawthorn‐infestingRhagoletis pomonellapopulations in Mexico: implications for sympatric host race formation

The genetic origins of species may not all trace to the same time and place as the proximate cause(s) for population divergence. Moreover, inherent gene-flow barriers separating populations may not all have evolved under the same geographical circumstances. These considerations have lead to a greater appreciation of the plurality of speciation: that one geographical mode for divergence may not always be sufficient to describe a speciation event. The apple maggot fly, Rhagoletis pomonella, a model system for sympatric speciation via host-plant shifting, has been a surprising contributor to the concept of speciation mode plurality. Previous studies have suggested that past introgression of inversion polymorphism from a hawthorn-fly population in the trans-Mexican volcanic belt (EVTM) introduced diapause life-history variation into a more northern fly population that subsequently contributed to sympatric host race formation and speciation in the United States (US). Here, we report results from a microsatellite survey implying (i) that volcanic activity in the eastern EVTM may have been responsible for the initial geographical isolation of the Mexican and northern hawthorn-fly populations c. 1.57 mya; and (ii) that flies in the Sierra Madre Oriental Mountains (SMO) likely served as a conduit for past gene flow from the EVTM into the US. Indeed, the microsatellite data suggest that the current US population may represent a range expansion from the northern SMO. We discuss the implications of these findings for sympatric race formation in Rhagoletis and speciation theory.

Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly, Rhagoletis pomonella.

Evidence suggests that the apple maggot, Rhagoletis pomonella (Diptera: Tephritidae) is undergoing sympatric speciation (i.e., divergence without geographic isolation) in the process of shifting and adapting to a new host plant. Prior to the introduction of cultivated apples (Malus pumila) in North America, R. pomonella infested the fruit of native hawthorns (Crataegus spp.). However, sometime in the mid-1800s the fly formed a sympatric race on apple. The recently derived apple-infesting race shows consistent allele frequency differences from the hawthorn host race for six allozyme loci mapping to three different chromosomes. Alleles at all six of these allozymes correlate with the timing of adult eclosion, an event dependent on the duration of the overwintering pupal diapause. This timing difference differentially adapts the univoltine fly races to an approximately 3- to 4-week difference in the peak fruiting times of apple and hawthorn trees, partially reproductively isolating the host races. Here, we report finding substantial gametic disequilibrium among allozyme and complementary DNA (cDNA) markers encompassing the three chromosomal regions differentiating apple and hawthorn flies. The regions of disequilibrium extend well beyond the previously characterized six allozyme loci, covering substantial portions of chromosomes 1, 2, and 3 (haploid n = 6 in R. pomonella). Moreover, significant recombination heterogeneity and variation in gene order were observed among single-pair crosses for each of the three genomic regions, implying the existence of inversion polymorphism. We therefore have evidence that genes affecting diapause traits involved in host race formation reside within large complexes of rearranged genes. We explore whether these genomic regions (inversions) constitute coadapted gene complexes and discuss the implications of our findings for sympatric speciation in Rhagoletis.

Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments.

Sympatric races of pea aphids on alfalfa and red clover are highly ecologically specialized and significantly reproductively isolated. Much of the restriction of gene flow between the specialized populations is due to habitat choice behavior of the winged colonizers (Via 1999). Here, we document additional pre- and postmating reproductive isolation through selection against migrants and hybrids in the parental environments. First, a group of randomly chosen genotypes from each race that were experimentally migrated between hosts had very low survival and reproduction on the alternate host relative to genotypes originating from that host (natives). Such selection against cross-host migrants forms a premating barrier to gene flow because it is likely to reduce migrant frequencies before the sexual forms are induced in the fall. Our reciprocal transplant experiment also shows that natural selection acts directly on individual migrants between the crops to favor host choice behavior: genotypes from each host suffered large losses of fitness when forced to migrate to the alternate host plant relative to the fitness they would have enjoyed had they been able to choose their native host. In a companion field study, sequential sampling throughout the summer in newly colonized fields of both alfalfa and clover revealed a decrease in the frequency of host-specific marker alleles characteristic of the alternate crop. These field data further support the hypothesis that selection disfavors migrants that cross between crops. Second, when two sets of F1 hybrids between the races were reciprocally tested on alfalfa and clover, both sets had significantly lower average fitness than the specialized parent in each of the two environments. This demographic selection against hybrids in the parental environments is a source of postmating reproductive isolation between the specialized races. Finally, significant genetic variation in fitness traits was seen among F1 hybrid genotypes from both crosses between alfalfa and clover specialists. Although this variation suggests that a generalized pea aphid could evolve, such generalists are not seen in field collections of these populations.

REPRODUCTIVE ISOLATION BETWEEN DIVERGENT RACES OF PEA APHIDS ON TWO HOSTS. II. SELECTION AGAINST MIGRANTS AND HYBRIDS IN THE PARENTAL ENVIRONMENTS

Sympatric races of pea aphids on alfalfa and red clover are highly ecologically specialized and significantly reproductively isolated. Much of the restriction of gene flow between the specialized populations is due to habitat choice behavior of the winged colonizers (Via 1999). Here, we document additional pre- and postmating reproductive isolation through selection against migrants and hybrids in the parental environments. First, a group of randomly chosen genotypes from each race that were experimentally migrated between hosts had very low survival and reproduction on the alternate host relative to genotypes originating from that host (natives). Such selection against cross-host migrants forms a premating barrier to gene flow because it is likely to reduce migrant frequencies before the sexual forms are induced in the fall. Our reciprocal transplant experiment also shows that natural selection acts directly on individual migrants between the crops to favor host choice behavior: genotypes from each host suffered large losses of fitness when forced to migrate to the alternate host plant relative to the fitness they would have enjoyed had they been able to choose their native host. In a companion field study, sequential sampling throughout the summer in newly colonized fields of both alfalfa and clover revealed a decrease in the frequency of host-specific marker alleles characteristic of the alternate crop. These field data further support the hypothesis that selection disfavors migrants that cross between crops. Second, when two sets of F1 hybrids between the races were reciprocally tested on alfalfa and clover, both sets had significantly lower average fitness than the specialized parent in each of the two environments. This demographic selection against hybrids in the parental environments is a source of postmating reproductive isolation between the specialized races. Finally, significant genetic variation in fitness traits was seen among F1 hybrid genotypes from both crosses between alfalfa and clover specialists. Although this variation suggests that a generalized pea aphid could evolve, such generalists are not seen in field collections of these populations.Corresponding Editor: C. Boggs

Reproductive Isolation between Sympatric Races of Pea Aphids. I. Gene Flow Restriction and Habitat Choice

Reproductive Isolation between Sympatric Races of Pea Aphids. I. Gene Flow Restriction and Habitat Choice

Toward a Molecular Genetic Linkage Map for the Apple Maggot Fly (Diptera: Tephritidae): Comparison of Alternative Strategies

Apple [Malus pumila (L.)] and hawthorn (Crataegus spp.) infesting populations of Rhagoletis pomonella Walsh are rapidly becoming a model system for the study of host plant specialization and sympatric race formation. Unfortunately, a major impediment to further progress in the Rhagoletis system is the lack of an adequate framework of genetic information. Here we report on the development of a molecular genetic linkage map for the fly and evaluate the relative merits of alternative strategies that we used to build the map. The most efficient method for detecting polymorphism in R. pomonella was based on screening a complementary DNA (cDNA) library for genetic variation. Twenty-four of the 98 cDNA clones that we attempted to analyze from plaques in the library displayed either restriction site (Alu I, Dde I, Sau 3A, or Taq I), fragment length, or single strand conformation polymorphism that could be mapped in R. pomonella and represented 25 different loci. Linkage group relationships were established for all 25 of these loci. Seven cDNA loci mapped to the 3 regions of the R. pomonella genome where the 6 allozyme loci with significant allele frequency differences between the host races are located. Furthermore, 5 of these 7 cDNA loci were in strong linkage disequilibrium with the allozyme loci residing within 2 of these 3 genomic regions, suggesting that the cDNA linkage map will be useful for dissecting the genetics of race formation in R. pomonella. Another successful strategy that we employed to map the locus glucose-6-phosphate dehijdrogenase (G-6-pdh) involved the use of a set of redundant primers that had been produced based on the conserved amino acid sequence of this gene. Surprisingly, a scheme based on screening plasmid libraries of randomly cloned restriction fragments was ineffective at detecting polymorphism, and it had an overall success rate of only 5.9% (3 mapped loci/51 low copy number clones screened for variation). In addition, application of random amplified polymorphic DNAs was unsuccessful in producing useful markers for the linkage map.

PARALLEL RACE FORMATION AND THE EVOLUTION OF MIMICRY INHELICONIUSBUTTERFLIES: A PHYLOGENETIC HYPOTHESIS FROM MITOCHONDRIAL DNA SEQUENCES

Mimicry has been a fundamental focus of research since the birth of evolutionary biology yet rarely has been studied from a phylogenetic perspective beyond the simple recognition that mimics are not similar due to common descent. The difficulty of finding characters to discern relationships among closely related and convergent taxa has challenged systematists for more than a century. The phenotypic diversity of wing pattens among mimetic Heliconius adds an additional twist to the problem, because single species contain more than a dozen radically different-looking geographical races even though the mimetic advantage is theoretically highest when all individuals within and between species appear the same. Mitochondrial DNA (mtDNA) offers an independent way to address these issues. In this study, Cytochrome Oxidase I and II sequences from multiple, parallel races of Heliconius erato and Heliconius melpomene are examined, to estimate intraspecific phylogeny and gauge sequence divergence and ages of clades among races within each species. Although phenotypes of sympatric races exhibit remarkable concordance between the two species, the mitochondrial cladograms show that the species have not shared a common evolutionary history. H. erato exhibits a basal split between trans- and cis-Andean groups of races, whereas H. melpomene originates in the Guiana Shield. Diverse races in either species appear to have evolved within the last 200,000 yr, and convergent phenotypes have evolved independently within as well as between species. These results contradict prior theories of the evolution of mimicry based on analysis of wing-pattern genetics.

Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly.

Models of sympatric speciation for phytophagous insects posit a central role for host plant-associated mating as a premating isolating mechanism in lieu of geographic barriers to gene flow. Here, by means of three mark-and-recapture studies, we confirm that host fidelity (i.e., the tendency of an insect to reproduce on the same host species that it used in earlier life-history stages) restricts gene flow between sympatric apple- and hawthorn-infesting races of Rhagoletis pomonella (Diptera: Tephritidae) to approximately 6% per generation. Genetically based differences in host preference, adult eclosion under the "correct" host species, and allochronic isolation contribute to host fidelity in various degrees in the races. The results verify that host-associated adaptation can produce reproductive isolation as a correlated character (a key premise of sympatric speciation). The study also represents one of the few or perhaps only example in animals where the intra-specific isolating effects of specific phenotypes have been quantified in nature.

Isolement reproducteur par homogamie entre deux « races d'habitat » sympatriques chez Drosophila melanogaster

Two races of D. melanogaster, morphologically identical, have been detected in the Brazzaville district (Congo). One (Loua = L), from the countryside, feeds and reproduces on manihot. The other (Kronenbourg = K) is found in the city bars and breweries, breeding on beer residues in empty bottles. These two populations can be distinguished by their genotypes at the Adh locus. The Kronenbourg population harbors 85 % of the F allele, while the frequency of this allele is less than 5 % in Loua. It is therefore easy to recognize them by mere electrophoresis. Under laboratory conditions, fertile FI and F2 hybrids are easily obtained. In natural conditions L and K remain separated. Behaviour plays probably a major role in reducing the gene flow through habitat choice and sexual behaviour. Sexual behaviour of these two races was analysed in laboratory. Sexual activity and mating choices were investigated by performing tests with four individuals (one male and one female of each race). In all tests, virgin adults were used. The L flies of both sexes exhibited a lower sexual activity than the K’s. Moreover, a significant homogamy independent of sexual activity was evidenced. It is the first time that such a phenomenon is found in D. melanogaster. This observation is of particular interest, since it concerns two sympatric races.

DIVERGENCE IN THE ENCHENOPA BINOTATA SAY COMPLEX (HOMOPTERA: MEMBRACIDAE) EFFECTED BY HOST PLANT ADAPTATION.

Intraspecific divergence is considered to be brought about by partial or complete geographic isolation in most animal groups which may lead to reproductive isolation (Mayr, 1963). However, evidence from a number of insect groups suggests intraspecific divergence and reproductive isolation may, under some conditions, occur in sympatric populations. Maynard Smith (1966) showed that disruptive selection acting on genotypes which influence habitat or host selection could lead to the formation of sympatric host races or species. Mechanisms such as allochronic shifts in the life history in crickets (Alexander and Bigelow, 1960; Alexander, 1968) or the adoption of new host plants by phytophagous insects may be involved in the formation of sympatric races or species. Host specificity of phytophagous or parasitic insects may establish initial conditions for sympatric speciation (Bush, 1975), but is not essential (Tauber and Tauber, 1977a, 1977b). Selection on insects restricted to deciduous hosts in geographic regions with drastic seasonal variation should produce insect life histories compatible with the host plant. Feeny (1970) demonstrated that the coordination of winter moth life history is geared to the availability of nutrients and defense system of the host plant. Many sap feeding homopterous insects such as aphids and scales are host plant specific showing adaptations to specific plants. For example, Edmunds and Alstad (1978) showed that differentiation in scale insects in response to the defense

PHYSIOLOGICAL ISOLATION IN COBITIDAE

1. The Ashida R. strain of the small race of the striated spinous loach, Cobitis taenia striata Ikeda, was crossed with the sympatric and allopatric strains of the middle race of the same subspecies. The two kinds of hybrids were compared in terms of male sterility and hybrid breakdown.2. Both F1 males derived from the crosses between sympatric races and those from the crosses between allopatric ones are almost completely sterile. There was scarcely any remarkable difference in abnormality of the spermatogenesis between the two kinds of F1 males.3. Both RF1 hybrids derived from the crosses between sympatric races and those from the crosses between allopatric ones partially showed inviability. Any significant difference in degree of inviability was scarcely found between the two kinds of RF1 hybrids.4. As far as the present study is concerned, it may be concluded that there is scarcely any positive evidence for the existence of especially strengthened hybrid sterility and hybrid breakdown in the contact regions of the two races.