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PubMed2003

Gene flow across species boundaries in sympatric, sexually deceptive Ophrys (Orchidaceae) species.

Orchids of the genus Ophrys (Orchidaceae) are pollinated by male bees and wasps through sexual deception. The Ophrys sphegodes group encompasses several closely related species that differ slightly in floral morphology and are pollinated by different solitary bee species. Populations representing different species of the O. sphegodes group often flower simultaneously in sympatry. To test whether gene flow across the species boundaries occurs in these sympatric populations, or whether they are reproductively isolated, we examined the distribution of genetic variation within and among populations and species of this group. We collected at each of five different localities in southern France and Italy two sympatric, co-flowering Ophrys populations, representing six Ophrys species in total. The six microsatellite loci surveyed were highly variable. Genetic differentiation among geographically distant populations of the same species was lower than differentiation among sympatric populations of different species. However, the strength of genetic differentiation among species was among the lowest reported for orchids. Genotype assignment tests and marker-based estimates of gene flow revealed that gene flow across species boundaries occurred and may account for the low observed differentiation among species. These results suggest that sexual deceit pollination in Ophrys may be less specific than thought, or that rare mistakes occur.

Cluster Analysis↗
PubMed2002

X-linked small GTPase and OXPHOS genes are candidates for the genetic basis of hybrid inviability in Drosophila.

Genetic studies on postmating reproductive isolation in Drosophila have suggested that the genetic basis of hybrid inviability is much less complex than the basis of hybrid sterility, and may be associated with defects affecting the cell cycle. Here I report the identification of a cluster of genes in the middle of the X chromosome of D. melanogaster, which may be responsible for the inviability of hybrids between Drosophila species. Genes from this cluster code for small Ras GTPases proteins, which are hypothesized here to interact with proteins involved in oxidative phosphorylation (OXPHOS), encoded by genes present within the same cluster. At least six genes influencing small Ras GTPases/OXPHOS activity are transcribed from the same strand across 35 kb genomic DNA. This interval is predicted to harbor genes which, when mutated, rescue otherwise inviable hybrids between D. melanogaster and its three most closely related species. Moreover, a total of 16 small GTPase/OXPHOS genes are found within 530 kb genomic DNA encompassing the above cluster. In D. melanogaster mutants which fully rescue lethal hybrids, major lesions have now been identified very near or within untranslated regions of two OXPHOS genes from the above cluster. These observations led to a hypothesis focusing on antagonistic co-evolution between biparentally inherited genes influencing putative GTPase/OXPHOS activity and mitochondrial genes encoding OXPHOS proteins. Alterations in some of these genes are postulated to override hybrid inviability, thus revealing a pathway which implicates mitotic genes as critical players in this barrier to reproduction.

Animals↗
PubMed2005

The genetic basis for fruit odor discrimination in Rhagoletis flies and its significance for sympatric host shifts.

Rhagoletis pomonella (Diptera: Tephritidae) use volatile compounds emitted from the surface of ripening fruit as important chemosensory cues for recognizing and distinguishing among alternative host plants. Host choice is of evolutionary significance in Rhagoletis because these flies mate on or near the fruit of their respective host plants. Differences in host choice based on fruit odor discrimination therefore result in differential mate choice and prezygotic reproductive isolation, facilitating sympatric speciation in the absence of geographic isolation. We test for a genetic basis for host fruit odor discrimination through an analysis of F2 and backcross hybrids constructed between apple-, hawthorn-, and flowering dogwood-infesting Rhagoletis flies. We recovered a significant proportion (30-65%) of parental apple, hawthorn, and dogwood fly response phenotypes in F2 hybrids, despite the general failure of F1 hybrids to reach odor source spheres. Segregation patterns in F2 and backcross hybrids suggest that only a modest number of allelic differences at a few loci may underlie host fruit odor discrimination. In addition, a strong bias was observed for F2 and backcross flies to orient to the natal fruit blend of their maternal grandmother, implying the existence of cytonuclear gene interactions. We explore the implications of our findings for the evolutionary dynamics of sympatric host race formation and speciation.

Animals↗
PubMed2005

Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation.

Female mate choice has often been proposed to play an important role in cases of rapid speciation, in particular in the explosively evolved haplochromine cichlid species flocks of the Great Lakes of East Africa. Little, if anything, is known in cichlid radiations about the heritability of female mating preferences. Entirely sympatric distribution, large ecological overlap and conspicuous differences in male nuptial coloration, and female preferences for these, make the sister species Pundamilia pundamilia and P. nyererei from Lake Victoria an ideally suited species pair to test assumptions on the genetics of mating preferences made in models of sympatric speciation. Female mate choice is necessary and sufficient to maintain reproductive isolation between these species, and it is perhaps not unlikely therefore, that female mate choice has been important during speciation. A prerequisite for this, which had remained untested in African cichlid fish, is that variation in female mating preferences is heritable. We investigated mating preferences of females of these sister species and their hybrids to test this assumption of most sympatric speciation models, and to further test the assumption of some models of sympatric speciation by sexual selection that female preference is a single-gene trait. We find that the differences in female mating preferences between the sister species are heritable, possibly with quite high heritabilities, and that few but probably more than one genetic loci contribute to this behavioural speciation trait with no apparent dominance. We discuss these results in the light of speciation models and the debate about the explosive radiation of cichlid fishes in Lake Victoria.

Animals↗
PubMed2002

The complex history of a gene proposed to participate in a sexual isolation mechanism in house mice.

Previous behavioral experiments showed that mouse salivary androgen-binding protein (ABP) was involved in interindividual recognition and might play a role in sexual isolation between house mouse (Mus musculus) subspecies. The pattern of evolution of Abpa, the gene for the alpha subunit of ABP, was found to be consistent with this hypothesis. Abpa apparently diverged rapidly between species and subspecies with a large excess of nonsynonymous substitutions, a lack of exon polymorphism within each of the three subspecies, and a lack of intron polymorphism in the one subspecies studied (M. musculus domesticus). Here we characterized the intron and exon sequence variations of this gene in house mouse populations from central Eurasia, a region yet unsampled and thought to be close to the cradle of the radiation of the subspecies. We also determined the intron and exon sequences in seven other species of the genus Mus. We confirmed the general pattern of rapid evolution by essentially nonsynonymous substitutions, both inter- and intraspecifically, supporting the idea that Darwinian selection has driven the evolution of this gene. We also observed a uniform intron sequence in five samples of M. musculus musculus, suggesting that a selective sweep might have occurred for that allele. In contrast to previous results, however, we found extensive intron and exon polymorphism in some house mouse populations from central Eurasia. We also found evidence for secondary admixture of the subspecies-specific alleles in regions of transition between the subspecies in central Eurasia. Furthermore, an abnormal intron phylogeny suggested that interspecific exchanges had occurred between the house mouse subspecies and three other Palearctic species. These observations appear to be at variance with the simple hypothesis that Abpa is involved in reproductive isolation. Although we do not rule out a role in recognition, the situation appears to be more complex than previously thought. Thus the selective mechanism behind the evolution of Abpa remains to be resolved, and we suggest that it may have changed during the recent colonization history of the house mouse.

Amino Acid Sequence↗
PubMed1995

Origin of sex for error repair. II. Rarity and extreme environments.

In a previous paper we studied the simultaneous, and at times conflicting, needs of coping with DNA damage, efficient cell replication, and the avoidance of cell mortality. These selective factors operated on sexual and asexual haploid and diploid populations that were reproductively isolated from one another. We concluded, in part, that a sexual type of cell could not expand from extreme rarity in populations dominated by asexual haploid and diploid cells. In the present paper we show that it is relatively easy for a rare sexual mutant to expand in a population dominated by asexual haploid cells if some matings occur between sexual and asexual cell types. We also study the persistence of sex in high mortality, high damage environments, in which neither the asexual diploid nor haploid can survive. The diploid cannot survive because its lower birth rate cannot overcome mortality and the haploid cannot survive because its birth rate cannot overcome gene damage. Sex can persist in these punishing environments by tuning the parameters of the sexual cycle, and the fusion and splitting rates, into a specified region, thereby reaping both benefits of damage repair and efficient replication.

Animals↗
PubMed2003

A role for the mismatch repair system during incipient speciation in Saccharomyces.

The cause of reproductive isolation between biological species is a major issue in the field of biology. Most explanations of hybrid sterility require either genetic incompatibilities between nascent species or gross physical imbalances between their chromosomes, such as rearrangements or ploidy changes. An alternative possibility is that genomes become incompatible at a molecular level, dependent on interactions between primary DNA sequences. The mismatch repair system has previously been shown to contribute to sterility in a hybrid between established yeast species by preventing successful meiotic crossing-over leading to aneuploidy. This system could also promote or reinforce the formation of new species in a similar manner, by making diverging genomes incompatible in meiosis. To test this possibility we crossed yeast strains of the same species but from diverse historical or geographic sources. We show that these crosses are partially sterile and present evidence that the mismatch repair system is largely responsible for this sterility.

Base Pair Mismatch↗
PubMed2006

Intraspecific competitive divergence and convergence under assortative mating.

Ecologically driven sympatric speciation has received much attention recently. We investigate a multilocus model of a quantitative trait that is under frequency-dependent selection caused by intraspecific competition and acts as mating character for assortment. We identify the conditions that lead to the establishment of reproductively isolated clusters. This may be interpreted as evolutionary splitting or sympatric speciation. In our model, there are parameters that independently determine the strength of assortment, the costs for being choosy, and the strength of frequency-dependent natural selection. Sufficiently strong frequency dependence leads to disruptive selection on the phenotypes. The population consists of (sexual) haploid individuals. If frequency dependence is strong enough to induce disruptive selection and costs are absent or low, the result of evolution depends in a distinctive nonlinear way on the strength of assortment: under moderately strong assortment, less genetic variation is maintained than under weak or strong assortment, and sometimes there is none at all. Evolutionary splitting occurs only if frequency dependence and assortment are both strong enough and costs are low. Even then, the evolutionary outcome depends on the genetics and the initial conditions. The roles of the number of loci, of linkage, and of asymmetric selection are also explored.

Animals↗
PubMed2000

Genetic analysis of speciation by means of introgression into Drosophila melanogaster.

In the last decade, the genetic basis of reproductive isolation has been shown to be surprisingly polygenic, and yet even the most efficient system currently in use could lend itself to molecular analysis only in highly selected cases. By extending the recent discovery of fertility rescue between Drosophila melanogaster and Drosophila simulans, we show that this hybridization can permit systematic and precise delineation of the genetic and molecular basis of speciation. In a region of 5% of the D. simulans genome introgressed into D. melanogaster, we discover at least six genes of hybrid male sterility and none for female sterility by deficiency mapping. A single case of hybrid inviability has been tracked down to a 3-Kb element that was inserted into the Cyclin E locus during species hybridization. The extent of interspecific genetic divergence underlying hybrid male sterility, especially in contrast with the low degree of inviability and female sterility, is far greater than expected from previous studies.

Animals↗
PubMed2003

Facultative symbionts are associated with host plant specialization in pea aphid populations.

The pea aphid, Acyrthosiphon pisum, shows significant reproductive isolation and host plant specialization between populations on alfalfa and clover in New York. We examine whether specialization is seen in pea aphids in California, and whether fitness on alternative host plants is associated with the presence of bacterial symbionts. We measured the fitness of alfalfa- and clover-derived aphids on both types of plants and found no evidence for specialization when all aphid lineages were considered simultaneously. We then screened all aphids for the presence of four facultative bacterial symbionts: PAR, PASS, PABS and PAUS. Aphids with PAUS were host-plant specialized, having twice as many offspring as other aphids on clover, and dying on alfalfa. Other aphids showed no evidence of specialization. Additionally, aphids with PABS had 50% more offspring than aphids with PASS when on alfalfa. Thus, specialist and generalist aphid lineages coexist, and specialization is symbiont associated. Further work will resolve whether PAUS is directly responsible for this variation in fitness or whether PAUS is incidentally associated with host-plant specialized aphid lineages.

Adaptation, Physiological↗
PubMed2003

Environmental influences on epistatic interactions: viabilities of cytochrome c genotypes in interpopulation crosses.

The genetic incompatibilities that underlie F2 hybrid breakdown and reproductive isolation between allopatric populations may be susceptible to environmental interactions. Here we show that epistatic interactions between cytochrome c (CYC) alleles and mitochondrial DNA (mtDNA) variation are dramatically influenced by environmental temperature in interpopulation hybrids of the copepod Tigriopus californicus. CYC is a nuclear-encoded gene that functionally interacts with electron transport system (ETS) complexes composed in part of mtDNA-encoded proteins. Previous studies have provided evidence for functional coadaptation between CYC and ETS complex IV (cytochrome c oxidase) and for cytoplasmic effects on the fitness of CYC genotype in copepod hybrids. In this study, selection on CYC genotype is shown to continue into advanced generation hybrids (F2-F8) increasing the likelihood that CYC itself is involved in the interaction (and not a linked factor). Relative viabilities varied markedly between copepods raised in two different temperature/light regimes. These results suggest that both intrinsic coadaptation and extrinsic selection will influence the outcome of natural hybridizations between populations. Furthermore, the results indicate that the fitness of particular hybrid genotypes depends on additional non-mtDNA encoded genes that interact with CYC.

Animals↗
PubMed2005

Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection.

It is now widely accepted that post-zygotic reproductive isolation is the result of negative epistatic interactions between derived alleles fixed independently at different loci in diverging populations (the Dobzhansky-Muller model). What is less clear is the nature of the loci involved and whether the derived alleles increase in frequency through genetic drift, or as a result of natural or sexual selection. If incompatible alleles are fixed by selection, transient polymorphisms will be rare and clines for these alleles will be steep where divergent populations meet. If they evolve by drift, populations are expected to harbour substantial genetic variation in compatibility and alleles will introgress across hybrid zones once they recombine onto a genetic background with which they are compatible. Here we show that variation in male sterility in a naturally occurring Chorthippus parallelus grasshopper hybrid zone conforms to the neutral expectations. Asymmetrical clines for male sterility have long tails of introgression and populations distant from the zone centre show significant genetic variation for compatibility. Our data contrast with recent observations on 'speciation genes' that have diverged as a result of strong natural selection.

Animals↗
PubMed2006

Reconstructing asymmetrical reproductive character displacement in a periodical cicada contact zone.

Selection against costly reproductive interactions can lead to reproductive character displacement (RCD). We use information from patterns of displacement and inferences about predisplacement character states to investigate causes of RCD in periodical cicadas. The 13-year periodical cicada Magicicada neotredecim exhibits RCD and strong reproductive isolation in sympatry with a closely related 13-year species, Magicicada tredecim. Displacement is asymmetrical, because no corresponding pattern of character displacement exists within M. tredecim. Results from playback and hybridization experiments strongly suggest that sexual interactions between members of these species were possible at initial contact. Given these patterns, we evaluate potential sources of selection for displacement. One possible source is 'acoustical interference', or mate-location inefficiencies caused by the presence of heterospecifics. Acoustical interference combined with the species-specificity of song pitch and preference appears to predict the observed asymmetrical pattern of RCD in Magicicada. However, acoustical interference does not appear to be a complete explanation for displacement in Magicicada, because our experiments suggest a significant potential for direct sexual interactions between these species before displacement. Another possible source of selection for displacement is hybrid failure. We evaluate the attractiveness of inferred hybrid mating signals, and we examine the viability of hybrid eggs. Neither of these shows strong evidence of hybrid inferiority. We conclude by presenting a model of hybrid failure related to life cycle differences in Magicicada.

Animals↗
PubMed2005

Speciation: more likely through a genetic or through a learned habitat preference?

A problem in understanding sympatric speciation is establishing how reproductive isolation can arise when there is disruptive selection on an ecological trait. One of the solutions that has been proposed is that a habitat preference evolves, and that mates are chosen within the preferred habitat. We present a model where the habitat preference can evolve either by means of a genetic mechanism or by means of learning. Employing an adaptive-dynamical analysis, we show that evolution proceeds either to a single population of specialists with a genetic preference for their optimal habitat, or to a population of generalists without a habitat preference. The generalist population subsequently experiences disruptive selection. Learning promotes speciation because it increases the intensity of disruptive selection. An individual-based version of the model shows that, when loci are completely unlinked and learning confers little cost, the presence of disruptive selection most probably leads to speciation via the simultaneous evolution of a learned habitat preference. For high costs of learning, speciation is most likely to occur via the evolution of a genetic habitat preference. However, the latter only happens when the effect of mutations is large, or when there is linkage between genes coding for the different traits.

Adaptation, Biological↗
PubMed2004

Experimental hybridisation between X0 and XY chromosome races in the grasshopper Podisma sapporensis Shir. (Orthoptera, Acrididae). I. Cytological analysis of embryos and F1 hybrids.

The results of experimental hybridisation between some chromosome subraces belonging to the X0 and XY chromosome races of the brachypterous grasshopper P. sapporensis are presented. Pre-zygotic reproductive isolation mechanisms in experimental pairs were not confirmed. In crossings of XY-standard x X0-standard and XY-standard x X0-Naganuma chromosome subraces, a zygotic barrier has been found. All embryos of XY-standard x X0-standard crosses and the vast majority of embryos of XY-standard x X0-Naganuma crosses were obtained from female diploid or haploid/diploid cells as a result of parthenogenesis. In very rare cases, when the zygotic barriers had been surmounted, normal embryo heterozygotes and a F1 hybrid generation were obtained in XY-standard x X0-Naganuma crosses. On the contrary, crosses between the XY-Tanno and X0-standard subraces gave viable offspring in spite of many chromosome differences such as a X-A translocation and fixed pericentric inversions in four pairs of autosomes. The results obtained do not support the hypothesis that chromosomal differences play a key role in restricting gene flow between X0 and XY races of P. sapporensis. The presence of crossing barriers explains the phenomena of the purity of the X0 and XY chromosomes races.

Animals↗
PubMed2005

Independent inheritance of preference and performance in hybrids between host races of Mitoura butterflies (Lepidoptera: Lycaenidae).

Divergent natural selection contributes to reproductive isolation among populations adapting to different habitats or resources if hybrids between populations are intermediate in phenotype and suffer an associated, environmentally dependent reduction in fitness. This prediction was tested using two host races of Mitoura butterflies. Thirty-five F1 hybrid and parental lines were created, larvae were raised on the two host plants, and oviposition preferences were assayed in choice arenas. Larvae from both reciprocal hybrid crosses suffered a host-specific reduction in performance: when reared on incense cedar, hybrid survival was approximately 30% less than the survival of pure lines of the cedar-associated host race. The performance of hybrid larvae reared on the other host, MacNab cypress, was not reduced relative to parental genotypes. Females from both reciprocal hybrid crosses preferred to oviposit on incense cedar, the same host that resulted in the reduced survival of hybrid larvae. Thus, dominance is implicated in the inheritance of traits involved in both preference and performance, which do not appear to be genetically linked in Mitoura butterflies. Gene flow between host races may be reduced because the correlation between preference and performance that was previously described in parental populations is essentially broken by hybridization.

Adaptation, Physiological↗
PubMed2005

Genetic continuity of brood-parasitic indigobird species.

Speciation in brood-parasitic indigobirds (genus Vidua) is a consequence of behavioural imprinting in both males and females. Mimicry of host song by males and host fidelity in female egg laying result in reproductive isolation of indigobirds associated with a given host species. Colonization of new hosts and subsequent speciation require that females occasionally lay eggs in the nests of novel hosts but the same behaviour may lead to hybridization when females parasitize hosts already associated with other indigobird species. Thus, retained ancestral polymorphism and ongoing hybridization are two alternative explanations for the limited genetic differentiation among indigobird species. We tested for genetic continuity of indigobird species using mitochondrial sequences and nuclear microsatellite data. Within West Africa and southern Africa, allopatric populations of the same species are generally more similar to each other than to sympatric populations of different species. Likewise, a larger proportion of genetic variation is explained by differences between species than by differences between locations in alternative hierarchical AMOVAS, suggesting that the rate of hybridization is not high enough to homogenize sympatric populations of different species or prevent genetic differentiation between species. Broad sharing of genetic polymorphisms among species, however, suggests that some indigobird species trace to multiple host colonization events in space and time, each contributing to the formation of a single interbreeding population bound together by songs acquired from the host species.

Africa↗
PubMed2002

Invasion of vacant niches and subsequent sympatric speciation.

An individual-based simulation study was conducted to examine the population dynamics of 'invasion of a vacant niche' and subsequent speciation (by reproductive isolation) when food resources are randomly distributed spatially within the habitat and the frequencies of different food types are bimodally distributed (i.e. smaller and larger sizes of food being most abundant). The initially vacant niche was that of unused larger sizes of food. When phenotypic variation for resource use (i.e. food sizes) was small in the initial population, and each female could choose a mate from anywhere in the habitat, the population could not invade the vacant niche. But when the dispersal distance of the offspring and the area within which a female could choose a mate were small (i.e. the genetic neighbourhood size was small), the population could, in most cases, evolve to use both smaller and larger food sizes and form sister species sympatrically, with each species utilizing one of the two niches (small and large sizes of food). When phenotypic variation in resource use in the initial population was large, the population could, in most cases, invade the vacant niche by evolving to use both smaller and larger sizes of food. The probability of speciation increased as the dispersal distance of offspring decreased. The results indicate that populations whose individuals have small Wright's genetic neighbourhoods may often exploit a vacant niche and diversify sympatrically in the process.

Animals↗