Speciation In Phytophagous Insects Research Articles

Host-plant adaptation as a driver of incipient speciation in the fall armyworm (Spodoptera frugiperda)

BackgroundDivergent selection on host-plants is one of the main evolutionary forces driving ecological speciation in phytophagous insects. The ecological speciation might be challenging in the presence of gene flow and assortative mating because the direction of divergence is not necessarily the same between ecological selection (through host-plant adaptation) and assortative mating. The fall armyworm (FAW), a major lepidopteran pest species, is composed of two sympatric strains, corn and rice strains, named after two of their preferred host-plants. These two strains have been hypothesized to undergo incipient speciation, based on (i) several lines of evidence encompassing both pre- and post-zygotic reproductive isolation, and (ii) the presence of a substantial level of genetic differentiation. Even though the status of these two strains has been established a long time ago, it is still yet to be found whether these two strains indeed exhibit a marked level of genetic differentiation from a large number of genomic loci. Here, we analyzed whole genome sequences from 56 FAW individuals either collected from pasture grasses (a part of the favored host range of the rice strain) or corn to assess the role of host-plant adaptation in incipient speciation.ResultsPrincipal component analysis of whole genome data shows that the pattern of divergence in the fall armyworm is predominantly explained by the genetic differentiation associated with host-plants. The level of genetic differentiation between corn and rice strains is particularly marked in the Z chromosome. We identified one autosomal locus and two Z chromosome loci targeted by selective sweeps specific to rice strain and corn strain, respectively. The autosomal locus has both increased DXY and FST while the Z chromosome loci had decreased DXY and increased FST.ConclusionThese results show that the FAW population structure is dominated by the genetic differentiation between corn and rice strains. This differentiation involves divergent selection targeting at least three loci, which include a locus potentially causing reproductive isolation. Taken together, these results suggest the evolutionary scenario that host-plant speciation is a driver of incipient speciation in the fall armyworm.

Invasion success of a scarab beetle within its native range: host range expansion versus host-shift.

Only recently has it been formally acknowledged that native species can occasionally reach the status of ‘pest’ or ‘invasive species’ within their own native range. The study of such species has potential to help unravel fundamental aspects of biological invasions. A good model for such a study is the New Zealand native scarab beetle, Costelytra zealandica (White), which even in the presence of its natural enemies has become invasive in exotic pastures throughout the country. Because C. zealandica still occurs widely within its native habitat, we hypothesised that this species has only undergone a host range expansion (ability to use equally both an ancestral and new host) onto exotic hosts rather than a host shift (loss of fitness on the ancestral host in comparison to the new host). Moreover, this host range expansion could be one of the main drivers of its invasion success. In this study, we investigated the fitness response of populations of C. zealandica from native and exotic flora, to several feeding treatments comprising its main exotic host plant as well as one of its ancestral hosts. Our results suggest that our initial hypothesis was incorrect and that C. zealandica populations occurring in exotic pastures have experienced a host-shift rather than simply a host-range expansion. This finding suggests that an exotic plant introduction can facilitate the evolution of a distinct native host-race, a phenomenon often used as evidence for speciation in phytophagous insects and which may have been instrumental to the invasion success of C. zealandica.

An Extreme Case of Plant–Insect Codiversification: Figs and Fig-Pollinating Wasps

It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant–insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale cophylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on an average, wasps had sequences from 77% of 6 genes (5.6 kb), figs had sequences from 60% of 5 genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based cophylogenetic analyses further support the codiversification hypothesis. Biogeographic analyses indicate that the present-day distribution of fig and pollinator lineages is consistent with a Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant–insect interactions of coordinated dispersal and long-term codiversification. [Biogeography; coevolution; cospeciation; host switching; long-branch attraction; phylogeny.]

Use of Host-Plant Trait Space by Phytophagous Insects during Host-Associated Differentiation: The Gape-and-Pinch Model

Ecological speciation via host shifting has contributed to the astonishing diversity of phytophagous insects. The importance for host shifting of trait differences between alternative host plants is well established, but much less is known about trait variationwithinhosts. I outline a conceptual model, the “gape-and-pinch” (GAP) model, of insect response to host-plant trait variation during host shifting and host-associated differentiation. I offer four hypotheses about insect use of plant trait variation on two alternative hosts, for insects at different stages of host-associated differentiation. Collectively, these hypotheses suggest that insect responses to plant trait variation can favour or oppose critical steps in herbivore diversification. I provide statistical tools for analysing herbivore trait-space use, demonstrate their application for four herbivores of the goldenrodsSolidago altissimaandS. gigantea, and discuss their broader potential to advance our understanding of diet breadth and ecological speciation in phytophagous insects.

Host-plant dependent wing phenotypic variation in the neotropical butterfly Heliconius erato

Most phytophagous insects feed on a single plant during development, and this may influence not only performance-linked traits, but also more subtle morphological differences. Insect-plant interactions are thus valuable for studying environmental influences on phenotypes. By using geometric morphometrics, we investigated the variation in forewing size and shape in the butterfly Heliconius erato phyllis reared on six species of passion vines (Passiflora spp.). We detected wing shape sexual dimorphism, for which the adaptive significance deserves further investigation. There was size as well as wing shape variation among individuals fed on different hosts. These subtle differences in shape were interpreted as environmental effects on development, which should be under weak natural selection for these traits, and therefore not strongly canalized. This result reinforces the role of plasticity on host-plant use, as well as the corresponding consequences on developmental variability among phytophagous insects. We propose that this variation can be an important factor in resource specialization and partner recognition, possibly triggering reproductive isolation and sympatric speciation in phytophagous insects. This interaction also shows itself as a good model for studying the role of environmental and interaction diversity in evolution.

Ecological speciation in phytophagous insects

AbstractDivergent natural selection has been shown to promote speciation in a wide range of taxa. For example, adaptation to different ecological environments, via divergent selection, can result in the evolution of reproductive incompatibility between populations. Phytophagous insects have been at the forefront of these investigations of ‘ecological speciation’ and it is clear that adaptation to different host plants can promote insect speciation. However, much remains unknown. For example, there is abundant variability in the extent to which divergent selection promotes speciation, the sources of divergent selection, the types of reproductive barriers involved, and the genetic basis of divergent adaptation. We review these factors here. Several findings emerge, including the observation that although numerous different sources of divergent selection and reproductive isolation can be involved in insect speciation, their order of evolution and relative importance are poorly understood. Another finding is that the genetic basis of host preference and performance can involve loci of major effect and opposing dominance, factors which might facilitate speciation in the face of gene flow. In addition, we raise a number of other recent issues relating to phytophagous insect speciation, such as alternatives to ecological speciation, the geography of speciation, and the molecular signatures of speciation. Throughout, we aim to both synthesize what is known, as well as highlight areas where future work is especially needed.

Counter-intuitive developmental plasticity induced by host quality

Adaptation to different hosts plays a central role in the evolution of specialization and speciation in phytophagous insects and parasites, and our ability to experimentally rank hosts by their quality is critical to research to understand these processes. Here we provide a counter-intuitive example in which growth is faster on poor quality hosts. The leaf beetles Oreina elongata and Oreina cacaliae share their host plant with the rust Uromyces cacaliae. Larvae reared on infected Adenostyles alliariae show reduced growth rate, reduced maximum weight and longer development time. However, they normally respond adaptively to the rust's mid-season arrival. When switched during development from healthy to infected leaves, larvae accelerate growth and reduce development time, but pupate at lower body weight. In this novel plant-insect-fungus interaction, infection forms the cue to trade off life-history traits in order to complete development within the brief alpine summer. It represents a novel mode of developmental plasticity, which is likely to be found in other host-parasite systems whenever host quality deteriorates due to multiple infection or ageing. This phenotypic plasticity would modify competition after co-infection and the mutual selection imposed by hosts and parasites, and creates a paradoxical negative correlation between growth rate and environmental quality.

Molecular evidence of host-associated genetic divergence in the holly leafminer Phytomyza glabricola (Diptera: Agromyzidae): apparent discordance among marker systems

Host races play a central part in understanding the role of host plant mediated divergence and speciation of phytophagous insects. Of greatest interest are host-associated populations that have recently diverged; however, finding genetic evidence for very recent divergences is difficult because initially only a few loci are expected to evolve diagnostic differences. The holly leafminer Phytomyza glabricola feeds on two hollies, Ilex glabra and I. coriacea, that are broadly sympatric throughout most of their ranges. The leafminer is often present on both host plants and exhibits a dramatic life history difference on the two hosts, suggesting that host races may be present. We collected 1393 bp of mitochondrial cytochrome oxidase I (COI) sequence and amplified fragment length polymorphism (AFLP) data (45 polymorphic bands) from sympatric populations of flies reared from the two hosts. Phylogenetic and frequency analysis of mitochondrial COI sequence data uncovered considerable variation but no structuring by the host plant, and only limited differentiation among geographical locations. In contrast, analysis of AFLP frequency data found a significant effect with host plant, and a much smaller effect with geographical location. Likewise, neighbour-joining analysis of AFLP data resulted in clustering by host plant. The AFLP data indicate that P. glabricola is most likely comprised of two host races. Because there were no fixed differences in mitochondrial or AFLP data, this host-associated divergence is likely to have occurred very recently. P. glabricola therefore provides a new sympatric system for exploring the role of geography and ecological specialization in the speciation of phytophagous insects.

Phylogenetics and phylogeography of the oak treehopper Platycotis vittata indicate three distinct North American lineages and a neotropical origin

Ecological differences including habitat, pollinators, and temporal separation between species and populations are important isolation barriers that can impede gene flows among evolving lineages, and subsequently lead to population divergence or speciation (Coyne and Orr, 2004). Temporal or allochronic speciation occurs when members of co-existing species or populations differ in breeding period that causes reproductive isolation as in the famous example of 13and 17-year periodical cicadas, Magicicada (Cooley et al., 2003). For insects like the apple maggot, Rhagoletis pomonella (Bush et al., 1989), the green lacewing, Chrysoperla plorabunda and C. downesi (Tauber and Tauber, 1977), and the treehopper, Enchenopa binotata (Wood, 1993a), the timing of reproduction can be greatly modified by their host-plant usage and the insect’s reproduction is strongly correlated with the plant phenology. Host shifting that changes life history timing thus plays an important role in reproductive isolation and speciation of phytophagous insects (Berlocher and Feder, 2002; Dres and Mallet, 2002). Treehoppers (Insecta: Hemiptera: Membracidae) are phytophagous insects that use their piercing and sucking mouthparts to feed on the phloem or xylem of plants (Wood, 1993b; Lin, 2006). The North American oak treehopper, Platycotis vittata (Fabricius) displays an extensive frontal horn dimorphism and color polymorphism in various life stages, between sexes, and throughout its geo-

Divergent preferences of Rhagoletis pomonella host races for olfactory and visual fruit cues

AbstractThe apple and hawthorn‐infesting host races of Rhagoletis pomonella Walsh (Diptera: Tephritidae) represent a model for incipient sympatric speciation. Recent studies have shown that apple and hawthorn flies differ in their responses to host‐fruit odor. Each host race preferentially orients to the volatile chemicals emanating from the surface of its natal fruit and is antagonized by non‐natal fruit volatiles. Fruit odor discrimination is evolutionarily important due to its contributory role in host‐specific mating, generating partial premating reproductive isolation between the races in sympatry. Visual cues are also involved in R. pomonella host searching, yet the extent to which they are used to discriminate between hosts has not been fully resolved, nor has their interaction with olfactory cues. Here, we report results from a series of two‐way choice experiments conducted in the field on resident apple and hawthorn flies at a site near Fennville, MI, USA. Four key findings emerged from the study: (1) both olfactory and (2) visual cues increased host discrimination of apple and hawthorn flies for their respective natal fruit, (3) the presence of a single appropriate volatile blend on a natal or non‐natal visual model generally increased the ability of flies to discriminate for their natal fruit, and (4) the presence of both natal and non‐natal olfactory cues on fruit models did not enhance host discrimination above levels observed for visual models alone. We discuss the implications of our results for interpreting the findings of two‐way host choice experiments and for sympatric speciation in phytophagous insects.

Sympatric speciation in phytophagous insects: moving beyond controversy?

Sympatric speciation is the splitting of one evolutionary lineage into two without the occurrence of geographic isolation. The concept has been intimately tied to entomology since the 1860s, when Benjamin Walsh proposed that many host-specific phytophagous insects originate by shifting and adapting to new host plant species. If true, sympatric speciation would have tremendous implications for our understanding of species and their origins, biodiversity (25-40% of all animals are thought to be phytophagous specialists), insect-plant coevolution, community ecology, phylogenetics, and systematics, as well as practical significance for the management of insect pests. During much of the twentieth century sympatric speciation was viewed as much less plausible than geographic (allopatric) speciation. However, empirical field studies, laboratory experiments, developments in population genetics theory, and phylogenetic and biogeographic data have all recently combined to shed a more favorable light on the process. We review the evidence for sympatric speciation via host shifting for phytophagous insects and propose a set of testable predictions for distinguishing geographic mode (allopatric versus sympatric) of divergence. Our conclusion is that sympatric speciation is a viable hypothesis. We highlight areas where more thorough testing is needed to move sympatric speciation into the realm of accepted scientific theory.

INSIGHT INTO SPECIATION FROM HISTORICAL DEMOGRAPHY IN THE PHYTOPHAGOUS BEETLE GENUS OPHRAELLA.

Speciation in phytophagous insects is commonly associated with shifts in host use. Using a phylogenetic framework to identify recently diverged taxa that have undergone a radical host shift, this study focuses on how reconstruction of the historical demography of a species, in conjunction with branching patterns between species, provides insight into mode of speciation. Analyses of mitochondrial cytochrome oxidase I sequences indicate that the leaf beetle Ophraella communa exhibits significant population structure, as shown by patterns of genealogical relationships among mitochondrial haplotypes and high FST -values. However, the absence of regional localization of old clades of haplotypes, negative Tajima's D, and unimodal rather than bimodal frequency distribution of the number of pairwise differences between sequences suggests an absence of long-term barriers to gene flow. Furthermore, we found no evidence of isolation by distance. This pattern of genetic variation is consistent with episodes of gene flow on a large geographic scale, perhaps owing to Pleistocene changes in climate. Ophraella communa and its sister species O. bilineata diverged during the early Pleistocene. The evidence of dynamic population structure in O. communa, potentially including episodic but massive gene flow, suggests that reproductive isolation evolved quite rapidly on a localized geographic scale, because speciation would probably have been reversed by gene flow if the evolution of reproductive isolation had been prolonged. That is, gene flow occasioned by range shifts during the Pleistocene would likely have interrupted speciation unless it occurred very rapidly. Sequence diversity implies a large effective population size (> 106 ) in both O. communa and O. bilineata. However, a model based on a drastic bottleneck did not have a lower likelihood than a model with no bottleneck, simply because the time since speciation has been great enough for coalescence to a single ancestor that existed after the speciation event. Sequence diversity in itself, without reference to the time since speciation, cannot provide evidence on the demography of speciation.

EVOLUTIONARY GENETICS OF OVIPOSITION PREFERENCE IN SWALLOWTAIL BUTTERFLIES.

Models of the evolution of host shifts and speciation in phytophagous insects are often built upon the assumption that host selection is under simple genetic control, perhaps even a single locus. The genetic basis for differences in host-plant preference by ovipositing insects was investigated using two closely related species of swallowtail butterfly, Papilio oregonius and P. zelicaon, which differ in the plant families on which females oviposit. Both species had been shown previously to vary within populations in host selection. A combination of analyses using reciprocal interspecific crosses and isofemale strains within populations indicated that oviposition preference in these species is determined significantly by one or more loci on the X chromosome, which female Lepidoptera inherit only paternally. Hence, preferences in hybrid females tended toward the paternal species. This is the first insect group for which partial control of oviposition preference has been localized onto a particular chromosome. In addition, one or more loci on another chromosome(s) appear to contribute to preference, as indicated by the partially intermediate preferences of some hybrid crosses. The overall differences in preference in the reciprocal interspecific hybrids were restricted to differences in the distribution of eggs laid among the local host plants of these two Papilio species; the reciprocal crosses did not differ in the small percentage of eggs laid on a novel potential host species. The variation in host selection found among the isofemale strains reinforces earlier results for these strains, indicating that there is genetic variation in host selection within these populations. Overall, the results indicate that the evolution of oviposition preference in these species involves genetic changes at two or more chromosomes with the X chromosome playing an important role in determining preference.

TRADEOFFS IN PERFORMANCE ON DIFFERENT HOSTS: EVIDENCE FROM WITHIN‐ AND BETWEEN‐SITE VARIATION IN THE BEETLE DELOYALA GUTTATA

Host races of phytophagous insects are sympatric populations that have different host preferences and between which gene flow is restricted because of the difference in host preference. Sympatric, host-associated sibling species are sympatric populations that use different host plants and that do not interbreed because of the presence of isolating mechanisms not related to host preference (Jaenike, 1981; see Mayr, 1970, and Bush, 1969, for slightly different definitions of these terms). Although the existence of host races and host-associated sibling species of phytophagous insects has been suspected for over 50 years (e.g., Thorpe, 1930), the evolutionary mechanism of host race formation remains controversial. In particular, there is disagreement about the importance of sympatric divergence in generating host races and species. White (1978) has argued that sympatric speciation must be invoked to explain, in part, the great diversity of specialized herbivorous insects, while Bush (1974, 1975) has forcefully advocated the operation of sympatric divergence in the creation of sympatric host races of tephritid flies. By contrast, Futuyma and Mayer (1980; see also Futuyma, 1983a) have argued that there is no reliable experimental evidence to support these claims and that models of sympatric speciation are based on assumptions that are probably not met by most phytophagous insects. Several authors have developed formal models of sympatric divergence and speciation (Maynard Smith, 1966; Dickinson and Antonovics, 1973; Caisse and Antonovics, 1978; Pimm, 1979; Felsenstein, 1981). Although these models do not account for the evolution of differences in host plant preference associated with purported sympatric speciation in phytophagous insects, Bush and Diehl (1983) and Rausher (1984) have suggested how modification of these models could remedy this problem. A common assumption of all these models is that fitness on one host is negatively correlated with fitness on a second. This type of negative correlation is manifested in these models in the assumption that genetic variation exists at loci that exhibit a genotype x host plant interaction, i.e., at loci at which some genotypes have high fitness on one host but low fitness on a second host while other genotypes have low fitness on the first but high fitness on the second host. This negative correlation seems to be necessary for sympatric speciation because it permits linkage disequilibrium to be established between loci influencing, say, viability on different hosts and loci influencing host preference. The resulting coadapted preference-viability gene complexes represent incipient host races or species. Moreover, the breakdown of these coadapted gene complexes by recombination provides the selection pressure that improves reproductive isolation, whether isolation is achieved via mating on the host (e.g., Bush, 1974, 1975) or by a separate assortative mating locus in linkage disequilibrium with loci affecting preference and fitness (e.g., Felsenstein, 1981). Without a crossing interaction, one homozygote genotype would have maximal fitness on both host species. Consequently, unless reproductive isolation were achieved instantaneously by a mutation

ECOLOGICAL GENERALISM IN DROSOPHILA FALLENI: GENETIC EVIDENCE.

The idea that speciation in phytophagous insects can occur sympatrically through the formation of host races was advanced over a century ago by Benjamin Walsh (1864), who postulated that conditioned preferences for plant species may gradually become genetically reinforced. Over the years, Walsh's model has been elaborated and refined by various workers (e.g., Thorpe, 1930, 1945; Dethier, 1954; Maynard Smith, 1966; Bush, 1969, 1974; Tauber and Tauber, 1977); and sufficient conditions for sympatric speciation were formulated by Maynard Smith (1966). In Maynard Smith's model, the first step in this process is the establishment of a stable polymorphism in a heterogeneous environment in which alternative alleles are selected in different niches (Levene, 1953). If then the polymorphism is coupled with strong habitat selection and mating within the niche, sympatric speciation may occur. Despite the continued interest of evolutionists in this mode of speciation and an extensive search for evidence of its occurrence (see Mayr, 1947, 1963, and 1970 for reviews), documented cases are rare (Bush, 1974), understandably, perhaps, because the probability of witnessing speciation events is small. However, the search for species at stages preceding speciation has been more successful. Polymorphisms maintained by disruptive selection on genetically variable host plants (Hatchett and Gallun, 1970), host selection based on larval conditioning (Craighead, 1921; Cushing, 1941; Huettel and Bush, 1972; Knerer and Atwood, 1973; Wiklund, 1974; Phillips and Barnes,