Glen R. Hood

Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow

Abstract Theory predicts that speciation‐with‐gene‐flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome‐wide impacts of host‐associated selection between hawthorn and apple host races of Rhagoletis pomonella (Diptera: Tephritidae), a model for contemporary speciation‐with‐gene‐flow. Allele frequency shifts of 32 455 SNPs induced in a selection experiment based on host phenology were genome wide and highly concordant with genetic divergence between co‐occurring apple and hawthorn flies in nature. This striking genome‐wide similarity between experimental and natural populations of R. pomonella underscores the importance of ecological selection at early stages of divergence and calls for further integration of studies of eco‐evolutionary dynamics and genome divergence.

GENETIC DIVERGENCE ALONG THE SPECIATION CONTINUUM: THE TRANSITION FROM HOST RACE TO SPECIES IN RHAGOLETIS (DIPTERA: TEPHRITIDAE)

Studies of related populations varying in their degrees of reproductive isolation can provide insights into speciation. Here, the transition from partially isolated host races to more fully separated sibling species is investigated by comparing patterns of genetic differentiation between recently evolved (∼150 generations) apple and ancestral hawthorn‐infesting populations of Rhagoletis pomonella to their sister taxon, the undescribed flowering dogwood fly attacking Cornus florida. No fixed or diagnostic private alleles differentiating the three populations were found at any of 23 microsatellites and 10 allozymes scored. Nevertheless, allele frequency differences were sufficient across loci for flowering dogwood fly populations from multiple localities to form a diagnosable genotypic cluster distinct from apple and hawthorn flies, indicative of species status. Genome‐wide patterns of differentiation were correlated between the host races and species pair comparisons along the majority of chromosomes, suggesting that similar disruptive selection pressures affect most loci. However, differentiation was more pronounced, with some additional regions showing elevated divergence, for the species pair comparison. Our results imply that Rhagoletis sibling species such as the flowering dogwood fly represent host races writ large, with the transition to species status primarily resulting from increased divergence of the same regions separating apple and hawthorn flies.

Ecological adaptation and reproductive isolation in sympatry: genetic and phenotypic evidence for native host races of Rhagoletis pomonella.

Ecological speciation with gene flow may be an important mode of diversification for phytophagous insects. The recent shift of Rhagoletis pomonella from its native host downy hawthorn (Crataegus mollis) to introduced apple (Malus domestica) in the northeastern United States is a classic example of sympatric host race formation. Here, we test whether R. pomonella has similarly formed host races on four native Crataegus species in the southern United States: western mayhaw (C. opaca), blueberry hawthorn (C. brachyacantha), southern red hawthorn (C. mollis var. texana) and green hawthorn (C. viridis). These four southern hosts differ from each other in their fruiting phenology and in the volatile compounds emitted from the surface of their fruits. These two traits form the basis of ecological reproductive isolation between downy hawthorn and apple flies in the north. We report evidence from microsatellite population surveys and eclosion studies supporting the existence of genetically differentiated and partially reproductively isolated host races of southern hawthorn flies. The results provide an example of host shifting and ecological divergence involving native plants and imply that speciation with gene flow may be commonly initiated in Rhagoletis when ecological opportunity presents itself.

Sequential divergence and the multiplicative origin of community diversity

Significance Understanding how new life forms originate is a central question in biology. Population divergence is usually studied with respect to how single lineages diverge into daughter taxa. However, populations may not always differentiate in isolation; divergence of one taxon could create new niche opportunities in higher trophic levels, leading to the sequential origin of many new taxa. Here, we show that this may be occurring for three species of parasitoid wasps attacking Rhagoletis fruit flies. As flies shift and adapt to new host plants, wasps follow suit and diverge in kind, resulting in a multiplicative increase of diversity as the effects of ecologically based divergent selection cascade through the ecosystem. Biodiversity therefore may potentially beget increasing levels of biodiversity. Phenotypic and genetic variation in one species can influence the composition of interacting organisms within communities and across ecosystems. As a result, the divergence of one species may not be an isolated process, as the origin of one taxon could create new niche opportunities for other species to exploit, leading to the genesis of many new taxa in a process termed “sequential divergence.” Here, we test for such a multiplicative effect of sequential divergence in a community of host-specific parasitoid wasps, Diachasma alloeum, Utetes canaliculatus, and Diachasmimorpha mellea (Hymenoptera: Braconidae), that attack Rhagoletis pomonella fruit flies (Diptera: Tephritidae). Flies in the R. pomonella species complex radiated by sympatrically shifting and ecologically adapting to new host plants, the most recent example being the apple-infesting host race of R. pomonella formed via a host plant shift from hawthorn-infesting flies within the last 160 y. Using population genetics, field-based behavioral observations, host fruit odor discrimination assays, and analyses of life history timing, we show that the same host-related ecological selection pressures that differentially adapt and reproductively isolate Rhagoletis to their respective host plants (host-associated differences in the timing of adult eclosion, host fruit odor preference and avoidance behaviors, and mating site fidelity) cascade through the ecosystem and induce host-associated genetic divergence for each of the three members of the parasitoid community. Thus, divergent selection at lower trophic levels can potentially multiplicatively and rapidly amplify biodiversity at higher levels on an ecological time scale, which may sequentially contribute to the rich diversity of life.

Geographic and Ecological Overlap of Parasitoid Wasps Associated with the Rhagoletis pomonella (Diptera: Tephritidae) Species Complex

ABSTRACT One of the fundamental questions in evolutionary ecology seeks to understand how new biodiversity is created and structured into communities. The apple maggot, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae), a model for rapid ecological speciation via host plant shifting for phytophagous insects, and its parasitoid community can offer insight into answering this and other related questions. Speciation of Rhagoletis also seems to be driving sequential speciation in a host specific parasitoid wasp Diachasma alloeum (Muesebeck) (Hymenoptera: Braconidae). However, biological and geographic information regarding D. alloeum and other parasitoids attacking flies in the genus Rhagoletis is sorely lacking, a problem that complicates the study of their evolution. Here, we present a synthesis of the geographic ranges and extended host associations of Rhagoletis-attacking parasitoids and test whether parasitoids can overlap in host use. In particular, we ask whether 1) wasps that co-occur in sympatry attack different life stages of the fly, 2) locally co-occurring wasps share some fly species in common but not others, 3) wasps differ in local abundance on those fly hosts they share in common, and 4) wasps vary on a regional scale in their geographic distributions. We use both collections and published records to answer the above-mentioned questions. A strong understanding of the Rhagoletis-attacking parasitoid distributions will facilitate future study of sequential radiation in this system.

The Geographic Distribution of Rhagoletis pomonella (Diptera: Tephritidae) in the Western United States: Introduced Species or Native Population?

ABSTBACT The apple maggot fly, Rhagoletis pomonella Walsh (Diptera: Tephritidae), is a major pest of commercially grown domesticated apple (Malus domestica Borkhausen) in North America. The shift of the fly from its native host hawthorn (Crataegus mollis) to apple in the eastern United States is often cited as an example of incipient sympatric speciation in action. However, R. pomonella is also present in the Pacific Northwest region of the United States where it infests apple, native black hawthorn (Crataegus douglasii), and introduced English ornamental hawthorn (C. monogyna). It is believed that R. pomonella was introduced to the Portland, OR, area via larval-infested apples from the east. The fly subsequently spread through the region, shifting onto black hawthorn and ornamental hawthorn as additional hosts as it spread. It is also possible, however, that R. pomonella is native to black hawthorn in the Pacific Northwest and switched to infest apple and ornamental hawthorn after the introduction of these two alternative hosts to the region. Here, we document the distribution of R. pomonella through the Pacific Northwest and Rocky Mountain states of the western United States to help clarify the origin (s) of the fly outside the eastern United States. We report a distribution pattern consistent with the hypothesis that R. pomonella was introduced to the Pacific Northwest via infested apples. In particular, the low levels or lack of C. dougliasii-infesting R. pomonella east of the Cascade Mountains in the states of Washington, OR, and Idaho implies that the fly is not native on black hawthorn and is of recent origin. We discuss the evolutionary and applied implications of the results with respect to our current understanding of host race formation and control for R. pomonella.

Developmental plasticity and reduced susceptibility to natural enemies following host plant defoliation in a specialized herbivore

Host-specific phytophagous insects that are short lived and reliant on ephemeral plant tissues provide an excellent system in which to investigate the consequences of disruption in the timing of resource availability on consumer populations and their subsequent interactions with higher tropic levels. The specialist herbivore, Belonocnema treatae (Hymenoptera: Cynipidae) induces galls on only newly flushed leaves of live oak, Quercus fusiformis. In central Texas (USA) episodic defoliation of the host creates variation in the timing of resource availability and results in heterogeneous populations of B. treatae that initiate development at different times. We manipulated the timing of leaf flush in live oak via artificial defoliation to test the hypothesis that a 6- to 8-week delay in the availability of resources alters the timing of this gall former’s life cycle events, performance and survivorship on its host, and susceptibility to natural enemies. B. treatae exhibits plasticity in development time, as the interval from egg to emergence was significantly reduced when gallers oviposited into the delayed leaf flush. As a consequence, the phenologies of gall maturation and adult emergence remain synchronized in spite of variation in the timing of resource availability. Per capita gall production and gall-former performance are not significantly affected by the timing of resource availability. The timing of resource availability and natural enemies interact, however, to produce strong effects on survivorship: when exposed to natural enemies, B. treatae developing in galls initiated by delayed oviposition exhibited an order-of-magnitude increase in survivorship. Developmental plasticity allows this gall former to circumvent disruptions in resource availability, maintain synchrony of life cycle events, and results in reduced vulnerability to natural enemies following defoliation of the host plant.

Divergent host-plant use promotes reproductive isolation among cynipid gall wasp populations

Ecological speciation occurs when reproductive isolation evolves as a consequence of divergent natural selection among environments. A direct prediction of this process is that ecologically divergent pairs of populations will exhibit greater reproductive isolation than ecologically similar pairs of populations. By comparing allopatric populations of the cynipid gall wasp Belonocnema treatae infesting Quercus virginiana and Quercus geminata, we tested the role that divergent host use plays in generating ecological divergence and sexual isolation. We found differences in body size and gall structure associated with divergent host use, but no difference in neutral genetic divergence between populations on the same or different host plant. We observed significant assortative mating between populations from alternative host plants but not between allopatric populations on the same host plant. Thus, we provide evidence that divergent host use promotes speciation among gall wasp populations.

Parallel Patterns of Morphological and Behavioral Variation among Host-Associated Populations of Two Gall Wasp Species

A powerful approach to address the general factors contributing to ecological speciation is to compare distantly related taxa that inhabit the same selective environments. In this design, similarities among taxa can elucidate general mechanisms of the process whereas differences may uncover specific factors important to the process for individual taxa. Herein, we present evidence of parallel patterns of morphological and behavioral variation among host-associated populations of two species of cynipid gall wasps, Belonocnema treatae and Disholcaspis quercusvirens, that each exhibit a life cycle intimately tied to the same two host plant environments, Quercus geminata and Q. virginiana. Across both gall-former species we find consistent differences in body size and gall morphology associated with host plant use, as well as strong differences in host plant preference, a measure of habitat isolation among populations. These consistent differences among taxa highlight the important role of host plant use in promoting reproductive isolation and morphological variation among herbivorous insect populations–a prerequisite for ecological speciation.

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.