Parasite diversity drives rapid host dynamics and evolution of resistance in a bacteria‐phage system

Host–parasite evolutionary interactions are typically considered in a pairwise species framework. However, natural infections frequently involve multiple parasites. Altering parasite diversity alters ecological and evolutionary dynamics as parasites compete and hosts resist multiple infection. We investigated the effects of parasite diversity on host–parasite population dynamics and evolution using the pathogen Pseudomonas aeruginosa and five lytic bacteriophage parasites. To manipulate parasite diversity, bacterial populations were exposed for 24 hours to either phage monocultures or diverse communities containing up to five phages. Phage communities suppressed host populations more rapidly but also showed reduced phage density, likely due to interphage competition. The evolution of resistance allowed rapid bacterial recovery that was greater in magnitude with increases in phage diversity. We observed no difference in the extent of resistance with increased parasite diversity, but there was a profound impact on the specificity of resistance; specialized resistance evolved to monocultures through mutations in a diverse set of genes. In summary, we demonstrate that parasite diversity has rapid effects on host–parasite population dynamics and evolution by selecting for different resistance mutations and affecting the magnitude of bacterial suppression and recovery. Finally, we discuss the implications of phage diversity for their use as biological control agents.     

Evolution of premating reproductive isolation among conspecific populations of the sea rock-pool beetle Ochthebius urbanelliae driven by reinforcing natural selection

How natural selection might be involved in speciation remains a fundamental question in evolutionary biology. When two or more species co-occur in the same areas, natural selection may favor divergence in mating traits. By acting in sympatric but not allopatric populations, natural selection can also affect mate choice within species and ultimately initiate speciation among conspecific populations. Here, we address this potential effect in the sea rock-pool beetles Ochthebius quadricollis and O. urbanelliae. The two species, which inhabit the Mediterranean coasts, co-occurr syntopically in an area along the Italian Tyrrhenian coast and completed reproductive isolation by reinforcement. In this article, through mating trials under laboratory conditions between conspecific populations, we found in O. quadricollis no deviations from random mating. Conversely, in O. urbanelliae, we found a clear pattern of premating isolation between the reinforced populations sympatric with O. quadricollis and those nonreinforced allopatric. This pattern is consistent with the view that natural selection, which completed the reproductive isolation between the two species in sympatry, led incidentally also to partial premating reproductive isolation (I(PSI) estimator from 0.683 to 0.792) between conspecific populations of O. urbanelliae. This case study supports an until recently underappreciated role of natural selection resulting from species interactions in initiating speciation.     

Evolution of reproductive isolation within a parasitic fungal species complex

Despite important advances in the last few years, the evolution of reproductive isolation (RI) remains an unresolved and critical gap in our understanding of speciation processes. In this study, we investigated the evolution of RI among species of the parasitic fungal species complex Microbotryum violaceum, which is responsible for anther smut disease of the Caryophyllaceae. We found no evidence for significant positive assortative mating by M. violaceum even over substantial degrees of genetic divergence, suggesting a lack of prezygotic isolation. In contrast, postzygotic isolation increased with the genetic distance between mating partners when measured as hyphal growth. Total RI, measured as the ability of the pathogen to infect and produce a diploid progeny in the host plant, was significantly and positively correlated with genetic distance, remaining below complete isolation for most of the species pairs. The results of this study, the first one on the time course of speciation in a fungus, are therefore consistent with previous works showing that RI generally evolves gradually with genetic distance, and thus presumably with time. Interestingly, prezygotic RI due to gamete recognition did not increase with genetic distance, in contrast to the pattern found in plants and animals.     

Deep sympatric mitochondrial divergence without reproductive isolation in the common redstart Phoenicurus phoenicurus

Mitochondrial DNA usually shows low sequence variation within and high sequence divergence among species, which makes it a useful marker for phylogenetic inference and DNA barcoding. A previous study on the common redstart (Phoenicurus phoenicurus) revealed two very different mtDNA haplogroups (5% K2P distance). This divergence is comparable to that among many sister species; however, both haplogroups coexist and interbreed in Europe today. Herein, we describe the phylogeographic pattern of these lineages and test hypotheses for how such high diversity in mtDNA has evolved. We found no evidence for mitochondrial pseudogenes confirming that both haplotypes are of mitochondrial origin. When testing for possible reproductive barriers, we found no evidence for lineage‐specific assortative mating and no difference in sperm morphology, indicating that they are not examples of cryptic species, nor likely to reflect the early stages of speciation. A gene tree based on a short fragment of cytochrome c oxidase subunit 1 from the common redstart and 10 other Phoenicurus species, showed no introgression from any of the extant congenerics. However, introgression from an extinct congeneric cannot be excluded. Sequences from two nuclear introns did not show a similar differentiation into two distinct groups. Mismatch distributions indicated that the lineages have undergone similar demographic changes. Taken together, these results confirm that deeply divergent mitochondrial lineages can coexist in biological species. Sympatric mtDNA divergences are relatively rare in birds, but the fact that they occur argues against the use of threshold mtDNA divergences in species delineation.     

Parasite host range and the evolution of host resistance

Parasite host range plays a pivotal role in the evolution and ecology of hosts and the emergence of infectious disease. Although the factors that promote host range and the epidemiological consequences of variation in host range are relatively well characterized, the effect of parasite host range on host resistance evolution is less well understood. In this study, we tested the impact of parasite host range on host resistance evolution. To do so, we used the host bacterium Pseudomonas fluorescens SBW25 and a diverse suite of coevolved viral parasites (lytic bacteriophage Φ2) with variable host ranges (defined here as the number of host genotypes that can be infected) as our experimental model organisms. Our results show that resistance evolution to coevolved phages occurred at a much lower rate than to ancestral phage (approximately 50% vs. 100%), but the host range of coevolved phages did not influence the likelihood of resistance evolution. We also show that the host range of both single parasites and populations of parasites does not affect the breadth of the resulting resistance range in a naïve host but that hosts that evolve resistance to single parasites are more likely to resist other (genetically) more closely related parasites as a correlated response. These findings have important implications for our understanding of resistance evolution in natural populations of bacteria and viruses and other host–parasite combinations with similar underlying infection genetics, as well as the development of phage therapy.     

Experimental evolution of viruses: Microviridae as a model system

φX174 was developed as a model system for experimental studies of evolution because of its small genome size and ease of cultivation. It has been used extensively to address statistical questions about the dynamics of adaptive evolution. Molecular changes seen during experimental evolution of φX174 under a variety of conditions were compiled from 10 experiments comprising 58 lineages, where whole genomes were sequenced. A total of 667 substitutions was seen. Parallel evolution was rampant, with over 50 per cent of substitutions occurring at sites with three or more events. Comparisons of experimentally evolved sites to variation seen among wild phage suggest that at least some of the adaptive mechanisms seen in the laboratory are relevant to adaptation in nature. Elucidation of these mechanisms is aided by the availability of capsid and pro-capsid structures for φX174 and builds on years of genetic studies of the phage life history.     

Evidence for sexual isolation as a prezygotic barrier to gene flow between morphologically divergent species of Rhagoletis fruit flies

1. Certain groups of fruit flies in the genus Rhagoletis (Diptera: Tephritidae) are exemplars for sympatric speciation via host plant shifting. Flies in these species groups are morphologically similar and overlap in their geographic ranges, yet attack different, non‐overlapping sets of host plants. Ecological adaptations related to differences in host choice and preference have been shown to be important prezygotic barriers to gene flow between these taxa, as Rhagoletis flies mate on or near the fruit of their respective host plants. Non‐host‐related assortative mating is generally absent or present at low levels between these sympatrically diverging fly populations. 2. However, some Rhagoletis taxa occasionally migrate to ‘non‐natal’ plants that are the primary hosts of other, morphologically differentiated fly species in the genus. These observations raise the question of whether sexual isolation may reduce courtship and copulation between morphologically divergent species of Rhagoletis flies, contributing to their prezygotic isolation along with host‐specific mating. 3. Using reciprocal multiple‐choice mating trials, we measured sexual isolation among nine species pairs of morphologically differentiated Rhagoletis flies. Complete sexual isolation was observed in eight of the nine comparisons, while partial sexual isolation was observed in the remaining comparison. 4. We conclude that sexual isolation can be an effective prezygotic barrier to gene flow contributing to substantial reproductive isolation between many morphologically distinct Rhagoletis species, even in the absence of differential host plant choice and host‐associated mating.     

Generalized selection to overcome innate immunity selects for host breadth in an RNA virus

Virus‐host coevolution has selected for generalized host defense against viruses, exemplified by interferon production/signaling and other innate immune function in eukaryotes such as humans. Although cell‐surface binding primarily limits virus infection success, generalized adaptation to counteract innate immunity across disparate hosts may contribute to RNA virus emergence potential. We examined this idea using vesicular stomatitis virus (VSV) populations previously evolved on strictly immune‐deficient (HeLa) cells, strictly immune competent (MDCK) cells, or on alternating deficient/competent cells. By measuring viral fitness in unselected human cancer cells of differing innate immunity, we confirmed that HeLa‐adapted populations were specialized for innate immune‐deficient hosts, whereas MDCK‐adapted populations were relatively more generalized for fitness on hosts of differing innate immune capacity and of different species origin. We also confirmed that HeLa‐evolved populations maintained fitness in immune‐deficient nonhuman primate cells. These results suggest that innate immunity is more prominent than host species in determining viral fitness at the host‐cell level. Finally, our prediction was inexact that selection on alternating deficient/competent hosts should produce innate viral generalists. Rather, fitness differences among alternating host‐evolved VSV populations indicated variable capacities to evade innate immunity. Our results suggest that the evolutionary history of innate immune selection can affect whether RNA viruses evolve greater host‐breadth.     

Expanding host specificity and pathogen sharing beyond viruses

Most emerging pathogens of humans can infect multiple host species (Woolhouse & Gowtage‐Sequeria, 2005). This simple fact has motivated multiple large‐scale, comparative analyses of the drivers of pathogen sharing and zoonotic pathogen richness among hosts as well as the factors determining the zoonotic potential of pathogens themselves. However, most of this work focuses on viruses, limiting a broader understanding of how host range varies within and between pathogen groups. In this issue of Molecular Ecology, Shaw et al. (2020) compile a comprehensive data set of host–pathogen associations across viruses and bacteria and test whether previous patterns observed in the former occur in the latter. They find most viruses and bacteria are specialists, and viruses are more likely to be generalists; however, generalist bacteria encompass multiple host orders, whereas viral sharing occurs more within host orders. Lastly, the authors demonstrate that many factors previously identified as predictors of zoonotic richness for viruses occur for bacteria and that host phylogenetic similarity is a primary determinant of cross‐species transmission. However, pathogen sharing with humans was more common and more weakly related to phylogenetic distance to Homo sapiens for bacteria compared to viruses, suggesting the former could pose greater spillover risks across host orders. This work represents a key advance in our understanding of host specificity and pathogen sharing beyond viruses.     

Experimental evolution of RNA versus DNA viruses

Based on their extremely high mutation rates, RNA viruses have been traditionally considered as the fastest evolving entities in nature. However, recent work has revealed that, despite their greater replication fidelity, single-stranded (ss) DNA viruses can evolve fast in a similar way. To further investigate this issue, we have compared the rates of adaptation and molecular evolution of ssRNA and ssDNA viruses under highly controlled laboratory conditions using the bacteriophages ΦX174, G4, f1, Qβ, SP, and MS2 as model systems. Our results indicate that ssRNA phages evolve faster than ssDNA phages under strong selective pressure, and that their extremely high mutation rates appear to be optimal for this kind of scenario. However, their performance becomes similar to that of ssDNA phages over the longer term or when the population is moderately well-adapted. Interestingly, the roughly 100-fold difference between the mutation rates of ssRNA and ssDNA phages yields less than a fivefold difference in adaptation and nucleotide substitution rates. The results are therefore consistent with the observation that, despite their lower mutation rates, ssDNA viruses can sometimes match the evolvability of RNA viruses.     

Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

The ubiquity of outcrossing in plants and animals is difficult to explain given its costs relative to self‐fertilization. Despite these costs, exposure to changing environmental conditions can temporarily favor outcrossing over selfing. Therefore, recurring episodes of environmental change are predicted to favor the maintenance of outcrossing. Studies of host–parasite coevolution have provided strong support for this hypothesis. However, it is unclear whether multiple exposures to novel parasite genotypes in the absence of coevolution are sufficient to favor outcrossing. Using the nematode Caenorhabditis elegans and the bacterial parasite Serratia marcescens, we studied host responses to parasite turnover. We passaged several replicates of a host population that was well‐adapted to the S. marcescens strain Sm2170 with either Sm2170 or one of three novel S. marcescens strains, each derived from Sm2170, for 18 generations. We found that hosts exposed to novel parasites maintained higher outcrossing rates than hosts exposed to Sm2170. Nonetheless, host outcrossing rates declined over time against all but the most virulent novel parasite strain. Hosts exposed to the most virulent novel strain exhibited increased outcrossing rates for approximately 12 generations, but did not maintain elevated levels of outcrossing throughout the experiment. Thus, parasite turnover can transiently increase host outcrossing. These results suggest that recurring episodes of parasite turnover have the potential to favor the maintenance of host outcrossing. However, such maintenance may require frequent exposure to novel virulent parasites, rapid rates of parasite turnover, and substantial host gene flow.     

Experimental evidence that source genetic variation drives pathogen emergence

A pathogen can readily mutate to infect new host types, but this does not guarantee successful establishment in the new habitat. What factors, then, dictate emergence success? One possibility is that the pathogen population cannot sustain itself on the new host type (i.e. host is a sink), but migration from a source population allows adaptive sustainability and eventual emergence by delivering beneficial mutations sampled from the source''s standing genetic variation. This idea is relevant regardless of whether the sink host is truly novel (host shift) or whether the sink is an existing or related, similar host population thriving under conditions unfavourable to pathogen persistence (range expansion). We predicted that sink adaptation should occur faster under range expansion than during a host shift owing to the effects of source genetic variation on pathogen adaptability in the sink. Under range expansion, source migration should benefit emergence in the sink because selection acting on source and sink populations is likely to be congruent. By contrast, during host shifts, source migration is likely to disrupt emergence in the sink owing to uncorrelated selection or performance tradeoffs across host types. We tested this hypothesis by evolving bacteriophage populations on novel host bacteria under sink conditions, while manipulating emergence via host shift versus range expansion. Controls examined sink adaptation when unevolved founding genotypes served as migrants. As predicted, adaptability was fastest under range expansion, and controls did not adapt. Large, similar and similarly timed increases in fitness were observed in the host-shift populations, despite declines in mean fitness of immigrants through time. These results suggest that source populations are the origin of mutations that drive adaptive emergence at the edge of a pathogen''s ecological or geographical range.     

Short-term rates of parasite evolution predict the evolution of host diversity

Coevolution with parasites has been implicated as an important factor driving the evolution of host diversity. Studies to date have focussed on gross effects of parasites: how host diversity differs in the presence vs. absence of parasites. But parasite-imposed selection is likely to show rapid variation through time. It is unclear whether short-term fluctuations in the strength of parasite-imposed selection tend to affect host diversity, because increases in host diversity are likely to be constrained by both the supply of genetic variation and ecological processes. We followed replicate populations of coevolving, initially isogenic, bacteria and phages through time, measuring host diversity (with respect to bacterial colony morphologies), host density and rates of parasite evolution. Both host density and time-lagged rates of parasite evolution were good independent predictors of the magnitude of bacterial within- and between-population diversities. Rapid parasite evolution and low host density decreased host within-population diversity, but increased between-population diversity. This study demonstrates that short-term changes in the rate of parasite evolution can predictably drive patterns of host diversity.     

Genetic isolation between two sympatric host-plant races of the European corn borer,Ostrinia nubilalis Hübner. I. Sex pheromone,moth emergence timing,and parasitism

Adaptation to different environments may be a powerful source of genetic differentiation between populations. The biological traits selected in each environment can pleiotropically induce assortative mating between individuals of these genetically differentiated populations. This situation may facilitate sympatric speciation. Successful host shifts in phytophagous insects provide some of the best evidence for the ecological speciation that occurs, or has occurred, in sympatry. The European corn borer, Ostrinia nubilalis (Lepidoptera: Crambidae), colonized maize after its introduction into Europe by humans about 500 years ago. In northern France, two sympatric host races feed on maize (Zea mays) and mugwort (Artemisia vulgaris), respectively. We investigated the factors involved in the genetic isolation of these two races at a field site near Paris, France. We identified two biological differences that might make a significant contribution to the genetic divergence between sympatric populations feeding on the two host plants. First, assortative mating may be due to differences in the moth emergence pattern between the two races: mugwort-race moths emerged on average 10 days earlier than maize-race moths. In addition, the males emerged earlier than females in both races. Hence, the likelihood of mating between maize-race males and mugwort-race females was higher than that of mating between mugwort-race males and maize-race females. Second, the females feeding on mugwort and maize produced sex pheromones with different E/Z isomeric ratios of delta-11-tetradecenyl acetate. This difference in mate recognition systems reinforces the potential for assortative mating in the two races. During the experiment, overwintering mortality was much lower on maize than on mugwort. This difference was due to a braconid parasitoid wasp, Macrocentrus cingulum, that killed more than 50% of the larvae overwintering on mugwort but did not infest larvae diapausing on maize. Hence, by colonizing maize, European corn borer populations probably escaped from numerous predators, competitors, and parasitoids, such as M. cingulum. This decrease in host-associated selection may have favored the colonization of this new host. Finally, throughout this experiment we observed selection at two allozyme loci (or at linked loci): Tpi and Mpi. The Tpi locus is tightly linked with the genes involved in the response of the male to the sex pheromone and in developmental timing. The location of these traits on the Z chromosome may play a role in shortening the time required for the evolution of premating barriers.     

Population differentiation and genetic variation in host choice among pea aphids from eight host plant genera

Habitat choice plays a critical role in the processes of host range evolution, specialization, and ecological speciation. Pea aphid, Acyrthosiphon pisum, populations from alfalfa and red clover in eastern North America are known to be genetically differentiated and show genetic preferences for the appropriate host plant. This species feeds on many more hosts, and here we report a study of the genetic variation in host plant preference within and between pea aphid populations collected from eight genera of host plants in southeastern England. Most host-associated populations show a strong, genetically based preference for the host plant from which they were collected. Only in one case (populations from Vicia and Trifolium) was there little difference in the plant preference spectrum between populations. All populations showed a significant secondary preference for the plant on which all the aphid lines were reared: broad bean, Vicia faba, previously suggested to be a "universal host" for pea aphids. Of the total genetic variance in host preference within our sample, 61% could be attributed to preference for the collection host plant and a further 9% to systematic differences in secondary preferences with the residual representing within-population genetic variation between clones. We discuss how a combination of host plant preference and mating on the host plant may promote local adaptation and possibly ecological speciation, and whether a widely accepted host could oppose speciation by mediating gene flow between different populations.     

Parallel host shifts in a bacterial plant pathogen suggest independent genetic solutions

While there are documented host shifts in many bacterial plant pathogens, the genetic foundation of host shifts is largely unknown. Xylella fastidiosa is a bacterial pathogen found in over 600 host plant species. Two parallel host shifts occurred—in Brazil and Italy—in which X. fastidiosa adapted to infect olive trees, whereas related strains infected coffee. Using 10 novel whole-genome sequences from an olive-infecting population in Brazil, we investigated whether these olive-infecting strains diverged from closely related coffee-infecting strains. Several single-nucleotide polymorphisms, many derived from recombination events, and gene gain and loss events separated olive-infecting strains from coffee-infecting strains in this clade. The olive-specific variation suggests that this event was a host jump with genetic isolation between coffee- and olive-infecting X. fastidiosa populations. Next, we investigated the hypothesis of genetic convergence in the host shift from coffee to olive in both populations (Brazil and Italy). Each clade had multiple mutations and gene gain and loss events unique to olive, yet no overlap between clades. Using a genome-wide association study technique, we did not find any plausible candidates for convergence. Overall, this work suggests that the two populations adapted to infect olive trees through independent genetic solutions.     

Evidence of reinforcement of premating isolation between two species of the genus Ochthebius (Coleoptera: Hydraenidae)

The increase in premating reproductive isolation between recently diverged and potentially interbreeding taxa resulting from selection against hybridization (reinforcement) is one of the most contentious issues in evolutionary biology. After many years of debate, its plausibility under various conditions has been shown by theoretical studies and some cases have been documented. At present, interest is arising about the frequency and importance of reinforcement in nature. Ochthebius quadricollis and Ochthebius sp. A are two hydraenid beetles inhabiting marine rock pools in the Mediterranean basin. By molecular analysis of a contact zone between the two species along the Italian Tyrrhenian coast, full reproductive isolation between the two species was evidenced. However, the finding of introgressed specimens at some diagnostic loci suggested that gene flow occurred in the past but then ceased. In this article, by analyzing species composition of mating couples collected in sympatric localities, we show the existence of strong assortative mating between the two species in nature. In laboratory multiple-choice mating trials, sympatric populations showed greater assortative mating than allopatric populations. Reinforcement is suggested as the most parsimonious hypothesis to explain the evolution of discriminative mate recognition systems occurring among O. quadricollis and Ochthebius sp. A under sympatric, but not allopatric, populations.     

Host‐associated pre‐mating reproductive isolation between host races of Acrocercops transecta: mating site preferences and effect of host presence on mating

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Experimental evolution: Assortative mating and sexual selection,independent of local adaptation,lead to reproductive isolation in the nematode Caenorhabditis remanei

Using experimental evolution, we investigated the contributions of ecological divergence, sexual selection, and genetic drift to the evolution of reproductive isolation in Caenorhabditis remanei. The nematodes were reared on two different environments for 100 generations. They were assayed for fitness on both environments after 30, 64, and 100 generations, and hybrid fitness were analyzed after 64 and 100 generations. Mating propensity within and between populations was also analyzed. The design allowed us to determine whether local adaptation was synchronous with pre‐ and postzygotic reproductive isolation. Prezygotic isolation evolved quickly but was unconnected with adaptation to the divergent environments. Instead, prezygotic isolation was driven by mate preferences favoring individuals from the same replicate population. A bottleneck treatment, meant to enhance the opportunity for genetic drift, had no effect on prezygotic isolation. Postzygotic isolation occurred in crosses where at least one population had a large fitness advantage in its “home” environment. Taken together, our results suggest that prezygotic isolation did not depend on drift or adaptation to divergent environments, but instead resulted from differences in sexual interactions within individual replicates. Furthermore, our results suggest that postzygotic isolation can occur between populations even when only one population has greater fitness in its home environment.     

Genetics, experience, and host-plant preference in Eurosta solidaginis: implications for host shifts and speciation

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.