Partial Reproductive Isolation Research Articles

Migration, isolation and hybridization in island crop populations: the case of Madagascar rice

Understanding how crop species spread and are introduced to new areas provides insights into the nature of species range expansions. The domesticated species Oryza sativa or Asian rice is one of the key domesticated crop species in the world. The island of Madagascar off the coast of East Africa was one of the last major Old World areas of introduction of rice after the domestication of this crop species and before extensive historical global trade in this crop. Asian rice was introduced in Madagascar from India, the Malay Peninsula and Indonesia approximately 800-1400 years ago. Studies of domestication traits characteristic of the two independently domesticated Asian rice subspecies, indica and tropical japonica, suggest two major waves of migrations into Madagascar. A population genetic analysis of rice in Madagascar using sequence data from 53 gene fragments provided insights into the dynamics of island founder events during the expansion of a crop species' geographic range and introduction to novel agro-ecological environments. We observed a significant decrease in genetic diversity in rice from Madagascar when compared to those in Asia, likely the result of a bottleneck on the island. We also found a high frequency of a unique indica type in Madagascar that shows clear population differentiation from most of the sampled Asian landraces, as well as differential exchange of alleles between Asia and Madagascar populations of the tropical japonica subspecies. Finally, despite partial reproductive isolation between japonica and indica, there was evidence of indica/japonica recombination resulting from their hybridization on the island.

Cattle ancestry in bison: explanations for higher mtDNA than autosomal ancestry

Understanding and documenting the process of hybridization and introgression between related species is a major focus of recent evolutionary research using molecular techniques. Many North American bison herds have cattle ancestry introduced by crossbreeding over a century ago. Molecular estimates of this ancestry have shown much higher levels for cattle mtDNA than for autosomal cattle genes. A large part of this difference appears to be the result of partial reproductive isolation between the two species where only bison bull x domestic cow crosses are successful, and all the surviving progeny are females. In addition, selection against autosomal cattle genes in bison may have contributed to differential levels of cattle ancestry. The impact of selection against cattle mtDNA and gene flow of bison mtDNA are examined to explain particular combinations of mtDNA and autosomal cattle ancestry. A bottleneck, after the level of cattle ancestry in bison was reduced to a low level, is consistent with the high variance over autosomal loci observed for cattle ancestry, and differential selection among cattle loci in bison does not need to be invoked. Further examination of the cattle genome in bison may shed light on whether these markers, or their associated regions, are indeed neutral.

Incomplete Reproductive Isolation in the Blue Mussel (Mytilus edulis and M. trossulus) Hybrid Zone in the Northwest Atlantic: Role of Gamete Interactions and Larval Viability

Reproductive isolation in free-spawning organisms may involve only small changes in the gamete surface molecules that control fertilization, linking gamete incompatibility and speciation. Most studies have focused on species in which natural hybrids are absent and reproductive isolation is complete, but how gamete incompatibility evolves remains unclear. Reproductive isolation is incomplete between two sympatric mussel species (Mytilus edulis, M. trossulus) that hybridize in nature. In this study prezygotic and postzygotic components of reproductive incompatibility were examined in laboratory crosses. Conspecific crosses showed significantly greater rates of fertilization than heterospecific crosses, although some females of both species showed heterospecific gamete compatibility. The proportion of fertilized eggs developing into normal larvae was not significantly different between conspecific and heterospecific crosses, but survival of normal larvae was greater for conspecific crosses. Mixed-species sperm experiments suggested that conspecific sperm preference may further limit hybridization. The different components of reproductive incompatibility and total incompatibility varied among females of both species. Although our study has shown that partial reproductive isolation between M. edulis and M. trossulus involves both prezygotic gamete interactions and postzygotic larval survival, further research is required to determine the potential role of gamete incompatibility in the evolution of complete reproductive isolation between these species.

Differences in defensive behaviour between host‐adapted races of the pea aphid

1. Host races, i.e. host‐adapted populations in partial reproductive isolation, have been reported in a growing number of insect herbivores including aphids. The pea aphid Acyrthosiphon pisum encompasses distinct races highly specialised on various Fabaceae plants. Races have been well documented at both the ecological and genetic level. However, little is known about possible behavioural differences between host races other than those involved in plant choice.2. The aim of this study was to determine whether pea aphid host races differ in the behavioural response to the aphid alarm pheromone that was used to simulate immediate predation risk. The behaviour of aphids towards a synthetic alarm pheromone applied in their vicinity was measured in several pea aphid clones originating from various legumes including Medicago sativa, Pisum sativum, Trifolium pratense, and Vicia faba. To control for the influence of plant traits, experiments were conducted on the preferred host plant and on the universal host plant Vicia faba.3. Host races differed in their defensive responses, with stronger behavioural responses in host races originating from M. sativa and T. pratense compared with those coming from P. sativum and V. faba. These differences in behaviour are inherent to the pea aphid host race but not dependent on the test plant.4. Our work shows that host‐plant specialisation may involve behavioural traits in addition to host choice. Possible mechanisms of how different defensive behaviours might have evolved are discussed.

Evolution of Neo-Sex Chromosomes inSilene diclinis

A small cluster of dioecious species in the plant genus Silene has evolved chromosomal sex determination and sex chromosomes relatively recently, within the last 10 million years (MY). Five dioecious Silene species (section Elisanthe) are very closely related (1-2 MY of divergence) and it was previously thought that all five have similar sex chromosomes. Here we demonstrate that in one of these species, Silene diclinis, the sex chromosomes have been significantly rearranged, resulting in the formation of neo-sex chromosomes. Fluorescence in situ hybridization with genic and repetitive probes revealed that in S. diclinis a reciprocal translocation has occurred between the ancestral Y chromosome and an autosome, resulting in chromosomes designated Y1 and Y2. Both Y1 and Y2 chromosomes are male specific. Y1 pairs with the X chromosome and with the autosome (the neo-X), which cosegregates with X. Y2 pairs only with the neo-X, forming a chain X-Y1-neo-X-Y2 in male meiosis. Despite very recent formation of the neo-sex chromosomes in S. diclinis, they are present in all surveyed individuals throughout the species range. Evolution of neo-sex chromosomes may be the cause of partial reproductive isolation of this species and could have been the isolating mechanism that drove speciation of S. diclinis.

Incipient ring speciation revealed by a migratory divide

Ever since Ernst Mayr (1942) called ring species the 'perfect demonstration of speciation', they have attracted much interest from researchers examining how two species evolve from one. In a ring species, two sympatric and reproductively isolated forms are connected by a long chain of intermediate populations that encircle a geographic barrier. Ring species have the potential to demonstrate that speciation can occur without complete geographic isolation, in contrast to the classic model of allopatric speciation. They also allow researchers to examine the causes of reproductive isolation in the contact zone and to use spatial variation to infer the steps by which speciation occurs. According to the classical definition, a ring species must have (i) gradual variation through a chain of populations connecting two divergent and sympatric forms, and (ii) complete or nearly complete reproductive isolation between the terminal forms. But evolutionary biologists now recognize that the process of speciation might often occur with some periods of geographic contact and hybridization between diverging forms; during these phases, even partial reproductive isolation can limit gene flow and permit further divergence to occur. In this issue Bensch et al. (2009) make an exciting and important contribution by extending the ring species concept to a case in which the divergence is much younger and not yet advanced to full reproductive isolation. Their study of geographic variation in willow warblers (Phylloscopus trochilus; Fig. 1) provides a beautiful example of gradual variation through a ring of populations connecting two forms that are partially reproductively isolated where they meet, possibly due to divergent migratory behaviours of the terminal forms.

Natural selection in action during speciation.

The role of natural selection in speciation, first described by Darwin, has finally been widely accepted. Yet, the nature and time course of the genetic changes that result in speciation remain mysterious. To date, genetic analyses of speciation have focused almost exclusively on retrospective analyses of reproductive isolation between species or subspecies and on hybrid sterility or inviability rather than on ecologically based barriers to gene flow. However, if we are to fully understand the origin of species, we must analyze the process from additional vantage points. By studying the genetic causes of partial reproductive isolation between specialized ecological races, early barriers to gene flow can be identified before they become confounded with other species differences. This population-level approach can reveal patterns that become invisible over time, such as the mosaic nature of the genome early in speciation. Under divergent selection in sympatry, the genomes of incipient species become temporary genetic mosaics in which ecologically important genomic regions resist gene exchange, even as gene flow continues over most of the genome. Analysis of such mosaic genomes suggests that surprisingly large genomic regions around divergently selected quantitative trait loci can be protected from interrace recombination by "divergence hitchhiking." Here, I describe the formation of the genetic mosaic during early ecological speciation, consider the establishment, effects, and transitory nature of divergence hitchhiking around key ecologically important genes, and describe a 2-stage model for genetic divergence during ecological speciation with gene flow.

Latitudinal Variation in Parasitoid Guild Composition and Parasitism Rates of North American Hawthorn InfestingRhagoletis

Rhagoletis pomonella (Diptera: Tephritidae) populations in North America have diverged by exploiting host plants with varying fruiting phenologies in environments that differ markedly in temperature and humidity. As a result, four genetically and ecologically distinct R. pomonella populations that display partial reproductive isolation have evolved. Host shifting by Rhagoletis and similar evolutionary histories could have had cascading effects across trophic levels, influencing the diversity and distribution of associated parasitoid guilds. To establish the basis for a future understanding of the possible effect of divergence in R. pomonella populations on the parasitoids attacking these flies, we surveyed parasitoids from five different species of hawthorns distributed over 15 states in México and 2 states in the midwestern United States. Emerging parasitoids were identified, parasitism rates were calculated, and regional fly and parasitoid emergence schedules were determined. Parasitism rate, emergence schedules, Shannon-Weiner diversity indexes, and species accumulation curves were compared across three main geographical regions. Parasitism levels varied greatly among regions from an overall high of 27.2% in the United States to 5.5% in the Sierra Madre Oriental (SMO) mountains of Mexico, to as low as 0.19% in the Eje Volcánico Trans Mexicano (EVTM). Shannon-Weiner diversity indexes showed that parasitoid species diversity was similar across the distribution range of R. pomonella in Mexico and the United States because of the fact that total parasitism was dominated by only two species, one of them recovered across the whole North American range of hawthorn infesting Rhagoletis. Nevertheless, eight parasitoids were found attacking R. pomonella in Mexico compared with only four collected in the United States. Only two diapausing parasitoid species were shared between the U.S. and Mexican R. pomonella populations: Utetes canaliculatus and Diachasmimorpha mellea. Interestingly, many subtropical parasitoid species, usually associated to flies in the subtropical genus Anastrepha, were recovered in the SMO in low numbers. The wide distribution of U. canaliculatus and D. mellea offers an ideal opportunity to test for a shared biogeography and co-evolution between fly and parasitoids. In this regard, one factor contributing to the success of U. canaliculatus seems to be the wasp's ability to modulate its eclosion time to track regional variation in hawthorn fruiting phenology and host (i.e., fly larvae) availability. Both R. pomonella and U. canaliculatus from southern sites emerged later than insects from northern populations, mirroring seasonal differences in hawthorn fruiting times across Mexico and the United States. These results suggest that molecular studies and crossing experiments could show, as they have for Rhagoletis, recent speciation events for parasitoid species of Nearctic origin that were found to be ecologically tracking environmentally driven divergence of their tephritid hosts.

ASSORTATIVE MATING PREFERENCES AMONG HYBRIDS OFFERS A ROUTE TO HYBRID SPECIATION

Homoploid speciation generates species without a change in chromosome number via introgressive hybridization and has been considered rare in animals. Heliconius butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. Heliconius heurippa has a color pattern that can be recreated by introgression of the H. melpomene red band into an H. cydno genetic background. Wild H. heurippa males show assortative mating based on color pattern and we here investigate the origin of this preference by studying first-generation backcross hybrids between H. melpomene and H. cydno that resemble H. heurippa. These hybrids show assortative mating preferences, showing a strong preference for their own color pattern over that of either parental species. This is consistent with a genetic basis to wing pattern preference and implies, first, that assortative mating preferences would facilitate the initial establishment of a homozygous hybrid color pattern by increasing the likelihood that early generation hybrids mate among themselves. Second, once established such a lineage would inherit assortative mating preferences that would lead to partial reproductive isolation from parental lineages.

VARIABLE PROGRESS TOWARD ECOLOGICAL SPECIATION IN PARAPATRY: STICKLEBACK ACROSS EIGHT LAKE-STREAM TRANSITIONS

Divergent selection between contrasting habitats can sometimes drive adaptive divergence and the evolution of reproductive isolation in the face of initially high gene flow. "Progress" along this ecological speciation pathway can range from minimal divergence to full speciation. We examine this variation for threespine stickleback fish that evolved independently across eight lake-stream habitat transitions. By quantifying stickleback diets, we show that lake-stream transitions usually coincide with limnetic-benthic ecotones. By measuring genetically based phenotypes, we show that these ecotones often generate adaptive divergence in foraging morphology. By analyzing neutral genetic markers (microsatellites), we show that adaptive divergence is often associated with the presence of two populations maintaining at least partial reproductive isolation in parapatry. Coalescent-based simulations further suggest that these populations have diverged with gene flow within a few thousand generations, although we cannot rule out the possibility of phases of allopatric divergence. Finally, we find striking variation among the eight lake-stream transitions in progress toward ecological speciation. This variation allows us to hypothesize that progress is generally promoted by strong divergent selection and limited dispersal across the habitat transitions. Our study thus makes a case for ecological speciation in a parapatric context, while also highlighting variation in the outcome.

Breeding experiments of hermatypic coralGalaxea fascicularis: partial reproductive isolation between colonies of different nematocyst types and enhancement of fertilization success by presence of parental colonies

Breeding experiments of hermatypic coral<i>Galaxea fascicularis</i>: partial reproductive isolation between colonies of different nematocyst types and enhancement of fertilization success by presence of parental colonies

Hybridization leads to host-use divergence in a polyphagous butterfly sibling species pair

Climate warming has lead to increased genetic introgression across a narrow hybrid zone separating the eastern and Canadian tiger swallowtails (Papilio glaucus and Papilio canadensis). This situation has led to the formation of an allochronically separated hybrid population with a delayed emerging phenotype or "late flight". Here, we assess how the recombination of the parental genomes that lead to this phenotype may have facilitated another major ecological shift, host-use divergence. We first contrast the ovipositional profiles of the late flight population to that of the parental species P. glaucus and P. canadensis. Subsequently we contrast the larval survival and growth of the late flight, a P. canadensis and a P. glaucus population, and a population from the northern edge of the hybrid zone on five hosts. Our results indicate that the ovipositional preference of this hybrid swarm is identical to that of the introgressing parental species, P. glaucus. Due to the absence of the preferred hosts of P. glaucus (Liriodendron tulipifera L. and Ptelea trifoliata L.) where the late flight occurs, this ovipositional pattern implies a functional specialization onto a secondary host of both parental species, Fraxinus americana L. In contrast, the larval host-use abilities represent a mixture of P. glaucus and P. canadensis, indicating divergence in larval host-use abilities has not taken place. However, high genetic variability (genetic coefficient of variation) is present for growth on F. americana in the late flight hybrid swarm and tradeoffs for larval performance on the preferred hosts of the parental species are evident; indicating a strong potential for future specialization in larval host-use abilities. This current scenario represents an instance where a shift in a major ecological trait, host use, is likely occurring as a byproduct of a shift in an unrelated trait (delayed emergence) leading to partial reproductive isolation.

A hybrid zone provides evidence for incipient ecological speciation inHeliconiusbutterflies

In Heliconius butterflies, it has been proposed that speciation occurs through a combination of divergence in ecological habitat preferences and mimetic colour patterns. Here we test this hypothesis by investigating a parapatric form of the widespread species Heliconius erato. Mendelian (colour patterns) and molecular genetic data permit us to address hypotheses about introgression and genetic differentiation between different populations. Combined analysis of colour pattern, microsatellite loci and mitochondrial DNA showed that Heliconius erato venus and Heliconius erato chestertonii form a bimodal hybrid zone implying partial reproductive isolation. In a sample of 121 individuals collected in sympatry, 25% were hybrids representing a significant deficit of heterozygotes compared to the Hardy-Weinberg expectation. Seven microsatellite loci, analysed for a subset of these individuals, showed marked differentiation between the parental taxa, and unambiguously identified two genotypic clusters concordant with our phenotypic classification of individuals. Mitochondrial DNA analysis showed H. erato venus as a monophyletic group well differentiated from H. erato chestertonii, implying a lack of historical introgression between the populations. Heliconius erato chestertonii is therefore an incipient species that maintains its integrity despite high levels of hybridization. Moreover, H. erato chestertonii is found at higher altitudes than other races of H. erato and has a distinct colour pattern and mimetic relationship. Hence, there are now two examples of parapatric incipient species related to H. erato, H. himera and H. erato chestertonii, both of which are associated with higher altitudes, more arid habitats and distinct mimetic relationships. This implies that parapatric habitat adaptation is a likely cause of speciation in this group.

EVOLUTION OF POLYPLOIDY AND THE DIVERSIFICATION OF PLANT–POLLINATOR INTERACTIONS

One of the major mechanisms of plant diversification has been the evolution of polyploid populations that differ from their diploid progenitors in morphology, physiology, and environmental tolerances. Recent studies have indicated that polyploidy may also have major effects on ecological interactions with herbivores and pollinators. We evaluated pollination of sympatric diploid and tetraploid plants of the rhizomatous herb Heuchera grossulariifolia (Saxifragaceae) along the Selway and Salmon Rivers of northern Idaho, USA, during four consecutive years. Previous molecular and ecological analyses had indicated that the tetraploid populations along these two river systems are independently derived and differ from each other in multiple traits. In each region, we evaluated floral visitation rate by all insect visitors, pollination efficacy of all major visitors, and relative contribution of all major pollinators to seed set. In both regions, diploid and tetraploid plants attracted different suites of floral visitors. Most pollination was attributable to several bee species and the moth Greya politella. Lasioglossum bees preferentially visited diploid plants at Lower Salmon but not at Upper Selway, queen Bombus centralis preferentially visited tetraploids at both sites, and worker B. centralis differed between sites in their cytotype preference. Hence, diploid and autotetraploid H. grossulariifolia plants act essentially as separate ecological species and may experience partial reproductive isolation through differential visitation and pollination by their major floral visitors. Overall the results, together with recent results from other studies, suggest that the repeated evolution of polyploidy in plants may contribute importantly to the structure and diversification of ecological interactions in terrestrial communities.

Sympatric, parapatric or allopatric: the most important way to classify speciation?

The most common classification of modes of speciation begins with the spatial context in which divergence occurs: sympatric, parapatric or allopatric. This classification is unsatisfactory because it divides a continuum into discrete categories, concentrating attention on the extremes, and it subordinates other dimensions on which speciation processes vary, such as the forces driving differentiation and the genetic basis of reproductive isolation. It also ignores the fact that speciation is a prolonged process that commonly has phases in different spatial contexts. We use the example of local adaptation and partial reproductive isolation in the intertidal gastropod Littorina saxatilis to illustrate the inadequacy of the spatial classification of speciation modes. Parallel divergence in shell form in response to similar environmental gradients in England, Spain and Sweden makes this an excellent model system. However, attempts to demonstrate 'incipient' and 'sympatric' speciation involve speculation about the future and the past. We suggest that it is more productive to study the current balance between local adaptation and gene flow, the interaction between components of reproductive isolation and the genetic basis of differentiation.

Heterospecific mating and partial prezygotic reproductive isolation in the planktonic marine copepods Centropages typicus and Centropages hamatus

Using three‐dimensional (3D) video observations in laboratory experiments, I describe interspecific and intergeneric mating behaviors and motility patterns of the common planktonic marine copepods Centropages typicus, Centropages hamatus, and Temora longicornis. These observations are then used to estimate heterospecific and conspecific male mate‐search volume rates and mate encounter rates in North Sea Centropages populations. Behavioral prezygotic reproductive isolation between Centropages species is incomplete, since males of each species pursued, contacted, captured, and, in rare cases, placed a spermatophore on the urosome of heterospecific females. T. longicornis males also detected the diffusible pheromone trail and pursued C. typicus females to the point of mate contact. Male mate‐search tracking behavior was equally effective on diffusible pheromone trails of heterospecific and conspecific females, indicating that pheromone and hydromechanical precontact mating cues lack species specificity. Males attempted mating with both heterospecific and conspecific females at high frequencies in the laboratory, and species recognition is inferred to occur through contact chemosensory cues or morphological incompatibility between species. Heterospecific mate encounter rates in the North Sea were maximal in late summer (August), up to~2,000 encounters m−3 d−1, and were comparable in magnitude to conspecific encounter rates during the same period. C. typicus females experience the highest incidence of heterospecific mating interactions, since they encounter heterospecific males at rates up to 100+ encounters female−1 d−1, ca. one order of magnitude higher than encounter rates with conspecifics. Heterospecific mating attempts may be a common feature of the reproductive ecology of planktonic copepods and may incur substantial fitness costs to the individuals involved.

THE GENETIC ARCHITECTURE OF REPRODUCTIVE ISOLATION IN LOUISIANA IRISES: POLLINATION SYNDROMES AND POLLINATOR PREFERENCES

In animal-pollinated plants, pollinator preferences for divergent floral forms can lead to partial reproductive isolation. We describe regions of plant genomes that affect pollinator preferences for two species of Louisiana Irises, Iris brevicaulis and Iris fulva, and their artificial hybrids. Iris brevicaulis and I. fulva possess bee and bird-pollination syndromes, respectively. Hummingbirds preferred I. fulva and under-visited both I. brevicaulis and backcrosses toward this species. Lepidopterans preferred I. fulva and backcrosses toward I. fulva, but also under-visited I. brevicaulis and I. brevicaulis backcrosses. Bumblebees preferred I. brevicaulis and F1 hybrids and rarely visited I. fulva. Although all three pollen vectors preferred one or the other species, these preferences did not prevent visitation to other hybrid/parental classes. Quantitative trait locus (QTL) mapping, in reciprocal BC1 mapping populations, defined the genetic architecture of loci that affected pollinator behavior. We detected six and nine QTLs that affected pollinator visitation rates in the BCIb and BCIf mapping populations, respectively, with as many as three QTLs detected for each trait. Overall, this study reflects the possible role of quantitative genetic factors in determining (1) reproductive isolation, (2) the pattern of pollinator-mediated genetic exchange, and thus (3) hybrid zone evolution.

Prebreeding in Common Bean and Use of Genetic Diversity from Wild Germplasm

ABSTRACTCommon bean (Phaseolus vulgaris L.) is the most widely consumed grain legume in the world. This cultigen was domesticated from wild P. vulgaris, an indeterminate viny plant, distributed from Mexico to Argentina in midaltitude neotropical and subtropical regions. To colonize such diverse ecological niches, the species possesses many adaptation traits and a wealth of genetic diversity. However, breeding programs are limited by the under‐utilization of the available genetic diversity because of the necessity of prebreeding exotic material. Due to partial reproductive isolation between the domesticated Andean and Mesoamerican gene pools, hybridizations between wild and domesticated types of P. vulgaris from the same gene pool offer greater potential to enhance the variation in the crop. Evaluations of wild P. vulgaris accessions have shown resistance to insects and diseases and higher N, Fe, and Ca content in seeds, which will ultimately contribute to improvements in nutritional quality and yield. Recurrent and inbred backcross methods are being used for the transfer of both qualitative and quantitative traits from wild into domesticated forms of P. vulgaris; specific data on yield and 100‐seed weight are presented. The prebreeding efforts will be enhanced by (i) information on gene pool origins, domestication syndrome traits, molecular diversity, and mapping data of the wild forms; (ii) indirect screening for biotic and abiotic stresses; and (iii) marker‐assisted selection.

PHYLOGENETIC EVIDENCE FOR MULTIPLE SYMPATRIC ECOLOGICAL DIVERSIFICATION IN A MARINE SNAIL

Parallel speciation can occur when traits determining reproductive isolation evolve independently in different populations that experience a similar range of environments. However, a common problem in studies of parallel evolution is to distinguish this hypothesis from an alternative one in which different ecotypes arose only once in allopatry and now share a sympatric scenario with substantial gene flow between them. Here we show that the combination of a phylogenetic approach with life-history data is able to disentangle both hypotheses in the case of the intertidal marine snail Littorina saxatilis on the rocky shores of Galicia in northwestern Spain. In this system, numerous phenotypic and genetic differences have evolved between two sympatric ecotypes spanning a sharp ecological gradient, and as aside effect of the former have produced partial reproductive isolation. A mitochondrial phylogeny of these populations strongly suggests that the two sympatric ecotypes have originated independently several times. Building upon earlier work demonstrating size-based assortative mating as the main contributor to reproductive isolation among ecotypes, our analysis provides strong evidence that divergent selection across a sharp ecological gradient promoted the parallel divergence of body size and shape between two sympatric ecotypes. Thus, divergent selection occurring independently in different populations has produced the marine equivalent of host races, which may represent the first step in speciation.

GENETICS, EXPERIENCE, AND HOST-PLANT PREFERENCE IN EUROSTA SOLIDAGINIS: IMPLICATIONS FOR HOST SHIFTS AND SPECIATION

Abstract Host‐associated mating is crucial in maintaining the partial reproductive isolation between the host races of Eurosta solidaginis (Diptera: Tephritidae), a fly that forms galls on Solidago altissima and S. gigantea. (We refer to flies reared from S. gigantea as gigantea flies and those reared from S. altissima as altissima flies.) We measured the host preference of males and females of both host races, F1 hybrids between the host races, F2, and backcrosses to both host races. Male and female altissima flies and female gigantea flies had high host fidelity, whereas male gigantea flies had low host fidelity. This result suggests that there may be gene flow between the host races due to nonassortative mating that occurs when male gigantea mate with altissima females on S. altissima. This indicates assortative‐mating mechanisms in addition to host‐associated mating are required to produce the partial reproductive isolation between the host races that has been observed. Nongenetic factors had no influence on host preference. Larval conditioning did not influence host preference: reciprocal F1 hybrids reared in S. altissima and S. gigantea both preferred S. gigantea. Adult experience had no impact on host preference: females preferred their natal host plant regardless of which host they encountered first as an adult. The hypothesis that maternal effects influence preferences was rejected because male and female flies did not show a consistent preference for the host plant of their mother. We also found no evidence that preference was a sex‐linked trait because F1 and backcrosses to the host races with different combinations of X chromosomes from the two host races preferred S. gigantea. Our results indicate that host preference is not determined by a large number of genes because preference of hybrids did not correspond to the proportion of the genome derived from each host race. The strength of the ovipuncture preference for S. gigantea by gigantea females, the females of both reciprocal F1 hybrids, the backcross to gigantea, and F2s indicates that preference is inherited nonadditively at a limited number of loci. The F1 female hybrids, however, had a weaker host preference for S. gigantea than the pure gigantea host race, indicating that there may be incomplete dominance or modifier loci. Males had different host preference patterns than females, with individual male gigantea and male F1 hybrids usually exhibiting preference exclusively for S. gigantea or S. altissima. One hypothesis explaining the difference in host preference between males and females is that the same gene influences both female and male host preference, but it is a sex‐influenced gene. Thus, males carrying the gene for S. gigantea preference have an intermediate host preference, whereas females have a strong host preference to S. gigantea. In summary, we found that the host preference that produces host‐associated mating is inherited nonadditively at a relatively small number of loci on autosomal genes. This mode of inheritance meets the assumptions of models of sympatric speciation, indicating that the host races could have evolved in sympatry.