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.
Here we report the genome sequence of the honeybee Apis mellifera, a key model for social behaviour and essential to global ecology through pollination. Compared with other sequenced insect genomes, the A. mellifera genome has high A+T and CpG contents, lacks major transposon families, evolves more slowly, and is more similar to vertebrates for circadian rhythm, RNA interference and DNA methylation genes, among others. Furthermore, A. mellifera has fewer genes for innate immunity, detoxification enzymes, cuticle-forming proteins and gustatory receptors, more genes for odorant receptors, and novel genes for nectar and pollen utilization, consistent with its ecology and social organization. Compared to Drosophila, genes in early developmental pathways differ in Apis, whereas similarities exist for functions that differ markedly, such as sex determination, brain function and behaviour. Population genetics suggests a novel African origin for the species A. mellifera and insights into whether Africanized bees spread throughout the New World via hybridization or displacement.
We characterized Apis mellifera in both native and introduced ranges using 1136 single-nucleotide polymorphisms genotyped in 341 individuals. Our results indicate that A. mellifera originated in Africa and expanded into Eurasia at least twice, resulting in populations in eastern and western Europe that are geographically close but genetically distant. A third expansion in the New World has involved the near-replacement of previously introduced "European" honey bees by descendants of more recently introduced A. m. scutellata ("African" or "killer" bees). Our analyses of spatial transects and temporal series in the New World revealed differential replacement of alleles derived from eastern versus western Europe, with admixture evident in all individuals.
Tephritid fruit flies belonging to the Rhagoletis pomonella sibling species complex are controversial because they have been proposed to diverge in sympatry (in the absence of geographic isolation) by shifting and adapting to new host plants. Here, we report evidence suggesting a surprising source of genetic variation contributing to sympatric host shifts for these flies. From DNA sequence data for three nuclear loci and mtDNA, we infer that an ancestral, hawthorn-infesting R. pomonella population became geographically subdivided into Mexican and North American isolates Ϸ1.57 million years ago. Episodes of gene flow from Mexico subsequently infused the North American population with inversion polymorphism affecting key diapause traits, forming adaptive clines. Sometime later (perhaps ؎1 million years), diapause variation in the latitudinal clines appears to have aided North American flies in adapting to a variety of plants with differing fruiting times, helping to spawn several new taxa. Thus, important raw genetic material facilitating the adaptive radiation of R. pomonella originated in a different time and place than the proximate ecological host shifts triggering sympatric divergence.
Rhagoletis pomonella is a model for incipient sympatric speciation (divergence without geographic isolation) by host-plant shifts. Here, we show that historically derived apple-and ancestral hawthorn-infesting host races of the fly use fruit odor as a key olfactory cue to help distinguish between their respective plants. In flight-tunnel assays and field tests, apple and hawthorn flies preferentially oriented to, and were captured with, chemical blends of their natal fruit volatiles. Because R. pomonella rendezvous on or near the unabscised fruit of their hosts to mate, the behavioral preference for apple vs. hawthorn fruit odor translates directly into premating reproductive isolation between the fly races. We have therefore identified a key and recently evolved (<150 years) mechanism responsible for host choice in R. pomonella bearing directly on sympatric host race formation and speciation.
Whether phytophagous insects can speciate in sympatry when they shift and adapt to new host plants is a controversial question. One essential requirement for sympatric speciation is that disruptive selection outweighs gene f low between insect populations using different host plants. Empirical support for host-related selection (i.e., fitness trade-offs) is scant, however. Here, we test for host-dependent selection acting on apple (Malus pumila)-and hawthorn (Crataegus spp.)-infesting races of Rhagoletis pomonella (Diptera: Tephritidae). In particular, we examine whether the earlier fruiting phenology of apple trees favors pupae in deeper states of diapause (or with slower metabolisms͞ development rates) in the apple f ly race. By experimentally lengthening the time period preceding winter, we exposed hawthorn race pupae to environmental conditions typically faced by apple f lies. This exposure induced a significant genetic response at six allozyme loci in surviving hawthorn f ly adults toward allele frequencies found in the apple race. The sensitivity of hawthorn f ly pupae to extended periods of warm weather therefore selects against hawthorn f lies that infest apples and helps to maintain the genetic integrity of the apple race by counteracting gene f low from sympatric hawthorn populations. Our findings confirm that postzygotic reproductive isolation can evolve as a pleiotropic consequence of host-associated adaptation, a central tenet of nonallopatric speciation. They also suggest that one reason for the paucity of reported fitness trade-offs is a failure to consider adequately costs associated with coordinating an insect's life cycle with the phenology of its host plant.Host plant-associated fitness trade-offs are critical for sympatric speciation in phytophagous insects (1). Fitness trade-offs refer to trait(s) or gene(s) that confer a selective advantage to an insect on one plant while incurring a cost on alternative plants. Such trade-offs are important because they can act as postzygotic barriers to gene flow between insect populations specialized on different host plants (1).There is currently little empirical evidence for host plantrelated fitness trade-offs in phytophagous insects (ref. 2, although see refs. 3-5 for some exceptions), which has raised questions concerning the likelihood of sympatric speciation (6). But many tests for fitness trade-offs have concentrated on larval feeding performance and the metabolic detoxification of plant secondary compounds while neglecting potential costs associated with coordinating an insect's life cycle with host plant phenology (7). Here, we test for fitness trade-offs in apple (Malus pumila)-and hawthorn (Crataegus spp.)-infesting populations of the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae) by examining whether and how differences in the fruiting phenologies (seasonalities) of apple and hawthorn trees affect the genetics of these flies.Previous studies have confirmed the status of apple and hawthorn populations of R. pomonella as g...
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