Integrating ancient patterns and current dynamics of insect–plant interactions: Taxonomic and geographic variation in herbivore specialization

Abstract The search for pattern in the ecology and evolutionary biology of insect–plant associations has fascinated biologists for centuries. High levels of tropical (low-latitude) plant and insect diversity relative to poleward latitudes and the disproportionate abundance of host-specialized insect herbivores have been noted. This review addresses several aspects of local insect specialization, host use abilities (and loss of these abilities with specialization), host-associated evolutionary divergence, and ecological (including “hybrid”) speciation, with special reference to the generation of biodiversity and the geographic and taxonomic identification of “species borders” for swallowtail butterflies (Papilionidae). From ancient phytochemically defined angiosperm affiliations that trace back millions of years to recent and very local specialized populations, the Papilionidae (swallowtail butterflies) have provided a model for enhanced understanding of localized ecological patterns and genetically based evolutionary processes. They have served as a useful group for evaluating the feeding specialization/physiological efficiency hypothesis. They have shown how the abiotic (thermal) environment interacts with host nutrirional suitability to generate “voltinism/suitability” gradients in specialization or preference latitudinally, and geographical mosaics locally. Several studies reviewed here suggest strongly that the oscillation hypothesis for speciation does have considerable merit, but at the same time, some species-level host specializations may lead to evolutionary dead-ends, especially with rapid environmental/habitat changes involving their host plants. Latitudinal gradients in species richness and degree of herbivore feeding specialization have been impacted by recent developments in ecological genetics and evolutionary ecology. Localized insect–plant associations that span the biospectrum from polyphenisms, polymorphisms, biotypes, demes, host races, to cryptic species, remain academically contentious, with simple definitions still debated. However, molecular analyses combined with ecological, ethological and physiological studies, have already begun to unveil some answers for many important ecological/evolutionary questions.     

Evolution of insect-plant relationships: chemical constraints, coadaptation, and concordance of insect/plant traits

Co-adaptations, co-evolution, and co-speciation between herbivores and their host plants have been topics of interest for several decades. Difficulties in deciphering these relationships as well as physiological, biochemical, and ecological adaptations of herbivorous insects themselves are discussed here in relation to biotic and abiotic environmental factors that create temporal as well as spatial mosaics of genetic variation. Hybridization was shown in swallowtail butterflies (Papilio) (Lepidoptera: Papilionidae) to produce some trait concordance, but mostly independent geographic trait clines (physiological, biochemical, and morphological). Strong and extensive genetic introgression of Liriodendron tulipifera detoxification abilities was documented northward across the hybrid zone, presumably as a result of regional climate warming only during the last 3–4 years. These and other genetic novelties produced by hybridization may be important in speciation processes, and they also emphasize the difficulties identifying appropriate taxonomic classifications for discussing any species concept. Host plant detoxification abilities (as `key innovations') are shown capable of rapid movement between different polyphagous herbivore species independently of the host plant availability and well beyond the insect species geographical range distribution. Part of the difficulty associated with ecologically categorizing herbivore species and identifying affiliated adaptations for host plant use may be related to independent movement of various `species-diagnostic' traits. Climate-driven local selection regimes could help generate the dynamic variation observed for co-adapted, co-evolved, or non-adapted genotypes, and may produce the confusing and changing patterns of geographic mosaics seen within and among closely related herbivores. Experimental analyses of several factors that could explain the asymmetrical shapes of trait clines across the hybrid zone for tiger swallowtail butterflies are discussed.     

Genetic divergence and hybrid speciation

Although the evolutionary importance of natural hybridization has been debated for decades, it has become increasingly clear that hybridization plays a fundamental role in the evolution of many plant and animal taxa, sometimes resulting in the formation of entirely new species. Although some hybrid species retain the base chromosome number of their parents, others combine the full chromosomal complements of their progenitors. Hybrid speciation can thus produce two fundamentally different types of evolutionary lineages, yet relatively little is known about the factors influencing ploidy level in hybrid neospecies. We estimated genetic divergence between species pairs that have given rise to homoploid and polyploid hybrid species and found that divergence is significantly greater for the parents of polyploids, even after controlling for potentially confounding factors. Our data thus provide the first direct evidence in support of the notion that the extent of genomic divergence between hybridizing species influences the likelihood of diploid versus polyploid hybrid speciation.     

Speciation as a sieve for ancestral polymorphism

Because they are considered rare, balanced polymorphisms are often discounted as crucial constituents of genome‐wide variation in sequence diversity. Despite its perceived rarity, however, long‐term balancing selection can elevate genetic diversity and significantly affect observed divergence between species. Here, we discuss how ancestral balanced polymorphisms can be “sieved” by the speciation process, which sorts them unequally across descendant lineages. After speciation, ancestral balancing selection is revealed by genomic regions of high divergence between species. This signature, which resembles that of other evolutionary processes, can potentially confound genomic studies of population divergence and inferences of “islands of speciation.”     

The genomic and ecological context of hybridization affects the probability that symmetrical incompatibilities drive hybrid speciation

Despite examples of homoploid hybrid species, theoretical work describing when, where, and how we expect homoploid hybrid speciation to occur remains relatively rare. Here, I explore the probability of homoploid hybrid speciation due to “symmetrical incompatibilities” under different selective and genetic scenarios. Through simulation, I test how genetic architecture and selection acting on traits that do not themselves generate incompatibilities interact to affect the probability that hybrids evolve symmetrical incompatibilities with their parent species. Unsurprisingly, selection against admixture at “adaptive” loci that are linked to loci that generate incompatibilities tends to reduce the probability of evolving symmetrical incompatibilities. By contrast, selection that favors admixed genotypes at adaptive loci can promote the evolution of symmetrical incompatibilities. The magnitude of these outcomes is affected by the strength of selection, aspects of genetic architecture such as linkage relationships and the linear arrangement of loci along a chromosome, and the amount of hybridization following the formation of a hybrid zone. These results highlight how understanding the nature of selection, aspects of the genetics of traits affecting fitness, and the strength of reproductive isolation between hybridizing taxa can all be used to inform when we expect to observe homoploid hybrid speciation due to symmetrical incompatibilities.     

GENETIC HITCHHIKING AND THE DYNAMIC BUILDUP OF GENOMIC DIVERGENCE DURING SPECIATION WITH GENE FLOW

A major issue in evolutionary biology is explaining patterns of differentiation observed in population genomic data, as divergence can be due to both direct selection on a locus and genetic hitchhiking. “Divergence hitchhiking” (DH) theory postulates that divergent selection on a locus reduces gene flow at physically linked sites, facilitating the formation of localized clusters of tightly linked, diverged loci. “Genome hitchhiking” (GH) theory emphasizes genome‐wide effects of divergent selection. Past theoretical investigations of DH and GH focused on static snapshots of divergence. Here, we used simulations assessing a variety of strengths of selection, migration rates, population sizes, and mutation rates to investigate the relative importance of direct selection, GH, and DH in facilitating the dynamic buildup of genomic divergence as speciation proceeds through time. When divergently selected mutations were limiting, GH promoted divergence, but DH had little measurable effect. When populations were small and divergently selected mutations were common, DH enhanced the accumulation of weakly selected mutations, but this contributed little to reproductive isolation. In general, GH promoted reproductive isolation by reducing effective migration rates below that due to direct selection alone, and was important for genome‐wide “congealing” or “coupling” of differentiation (F_ST) across loci as speciation progressed.     

Interactions between Papilionidae and ancient Australian Angiosperms: evolutionary specialization or ecological monophagy?

The evolution of host range for insect herbivores involves many behavioral, physiological, and biochemical adaptations that often lead to locally specialized populations or species. Such specialization may be constrained by ecological factors (e.g., local host availability) or by evolutionary factors (e.g., phylogenetic divergence in behavioral, physiological, or biochemical detoxification enzymes; and potential inabilities to return to ancestral hosts). While insect adaptations to new hosts can be rapid, ancient detoxification systems may persist in some lineages of swallowtail butterflies (Papilionidae) for millions of years. Here, we test various species of specialized species/populations of Papilionidae (Lepidoptera) from North America and from Australia on an array of Australian host plant families in order to determine whether the current feeding constraints reflect loss of capabilities to recognize and use hosts other than their current (local) favorites. We selected two species of Lauraceae specialists (Papilio troilus L. and Papilio palamedes Drury) from North America and one locally specialized population of Papilio glaucus L. that only uses one plant species in the Magnoliaceae in Florida. We also examined three species/populations of Australian swallowtails for comparison, including the Monimiaceae‐specialized Graphium macleayanum moggana L. E. Couchman, the Rutaceae‐specialized Papilio aegeus Donovan, and the Annonaceae‐specialized Graphium eurypylus L. Our aim was to determine whether neonate larvae of these six specialists could survive on any plants other than their currently favored species. While the Lauraceae specialists could use nothing else and were thus evolutionarily constrained, the Magnoliaceae‐, Rutaceae‐, and Monimiaceae specialists all had common abilities to accept, feed, and grow on plants in the Lauraceae, Monimiaceae, Magnoliaceae, and Rutaceae families. Even the Annonaceae specialist was discovered using Magnoliaceae in the field, suggesting existence here also of both flexiblity in preferences and detoxification abilities and ‘ecological monophagy’.     

THE EFFICACY OF DIVERGENCE HITCHHIKING IN GENERATING GENOMIC ISLANDS DURING ECOLOGICAL SPECIATION

Genes under divergent selection flow less readily between populations than other loci. This observation has led to verbal “divergence hitchhiking” models of speciation in which decreased interpopulation gene flow surrounding loci under divergent selection can generate large regions of differentiation within the genome (genomic islands). The efficacy of this model in promoting speciation depends on the size of the region affected by divergence hitchhiking. Empirical evidence is mixed, with examples of both large and small genomic islands. To address these empirical discrepancies and to formalize the theory, we present mathematical models of divergence hitchhiking, which examine neutral differentiation around selected sites. For a single locus under selection, regions of differentiation do not extend far along a chromosome away from a selected site unless both effective population sizes and migration rates are low. When multiple loci are considered, regions of differentiation can be larger. However, with many loci under selection, genome‐wide divergence occurs and genomic islands are erased. The results show that divergence hitchhiking can generate large regions of differentiation, but that the conditions under which this occurs are limited. Thus, speciation may often require multifarious selection acting on many, isolated and physically unlinked genes. How hitchhiking promotes further adaptive divergence warrants consideration.     

WIDESPREAD HOST‐DEPENDENT HYBRID UNFITNESS IN THE PEA APHID SPECIES COMPLEX

Linking adaptive divergence to hybrid unfitness is necessary to understand the ecological factors contributing to reproductive isolation and speciation. To date, this link has been demonstrated in few model systems, most of which encompass ecotypes that occupy relatively early stages in the speciation process. Here we extend these studies by assessing how host‐plant adaptation conditions hybrid fitness in the pea aphid, Acyrthosiphon pisum. We made crosses between and within five pea aphid biotypes adapted to different host plants and representing various stages of divergence within the complex. Performance of F1 hybrids and nonhybrids was assessed on a “universal” host that is favorable to all pea aphid biotypes in laboratory conditions. Although hybrids performed equally well as nonhybrids on the universal host, their performance was much lower than nonhybrids on the natural hosts of their parental populations. Hence, hybrids, rather than being intrinsically deficient, are maladapted to their parents’ hosts. Interestingly, the impact of this maladaptation was stronger in certain hybrids from crosses involving the most divergent biotype, suggesting that host‐dependent postzygotic isolation has continued to evolve late in divergence. Even though host‐independent deficiencies are not excluded, hybrid maladaptation to parental hosts supports the hypothesis of ecological speciation in this complex.     

Island floras as model systems for studies of plant speciation: Prospects and challenges

Oceanic islands have long been called natural laboratories for studying evolution because they are geologically young, isolated, dynamic areas with diverse habitats over small spatial scales. Volcanic substrates of different ages permit the study of different stages of divergence and speciation within plant lineages. In addition to divergence, the dynamic island setting is conducive to hybridization. Discussion will focus on the potential of systematic/ecological studies, in combination with genomic data from high throughput sequencing and an ever‐increasing array of analytical techniques, for studying evolution in island plants. These studies may include: generation of highly resolved phylogenies to clarify the biogeography of speciation and whether divergence has occurred with or without gene flow; identification of the barriers to gene flow (extrinsic vs. intrinsic) of importance during divergence; documentation of historical and current hybridization events within island lineages; and elucidation of the genomic composition and ecology of hybrid populations in order to infer the evolutionary consequences of hybridization, such as the origin of stabilized homoploid hybrid species.     

Phoretic dispersal influences parasite population genetic structure

Dispersal is a fundamental component of the life history of most species. Dispersal influences fitness, population dynamics, gene flow, genetic drift and population genetic structure. Even small differences in dispersal can alter ecological interactions and trigger an evolutionary cascade. Linking such ecological processes with evolutionary patterns is difficult, but can be carried out in the proper comparative context. Here, we investigate how differences in phoretic dispersal influence the population genetic structure of two different parasites of the same host species. We focus on two species of host‐specific feather lice (Phthiraptera: Ischnocera) that co‐occur on feral rock pigeons (Columba livia). Although these lice are ecologically very similar, “wing lice” (Columbicola columbae) disperse phoretically by “hitchhiking” on pigeon flies (Diptera: Hippoboscidae), while “body lice” (Campanulotes compar) do not. Differences in the phoretic dispersal of these species are thought to underlie observed differences in host specificity, as well as the degree of host–parasite cospeciation. These ecological and macroevolutionary patterns suggest that body lice should exhibit more genetic differentiation than wing lice. We tested this prediction among lice on individual birds and among lice on birds from three pigeon flocks. We found higher levels of genetic differentiation in body lice compared to wing lice at two spatial scales. Our results indicate that differences in phoretic dispersal can explain microevolutionary differences in population genetic structure and are consistent with macroevolutionary differences in the degree of host–parasite cospeciation.     

Significance of a new field oviposition record for Graphium eurypylus (L.) (Lepidoptera: Papilionidae) on Michelia champaca (Magnoliaceae)

Abstract  Phytochemical similarities among ancient Angiosperms presumably played a role in the ecological and evolutionary diversification of the swallowtail butterflies (Papilionidae). Host family feeding specialisation is typical of most Papilionidae species, but field records of oviposition are rare for most swallowtail butterflies. It is even more uncommon to witness oviposition and larval feeding on new host plant species, especially in plant families not previously reported for the butterfly species. Oviposition by a female on a new host, or even on a toxic plant, may represent ancestral behaviour (with a loss of larval acceptance, detoxification or processing abilities) or novel behaviour (providing genetic variation for a potential expansion of host range, or host shift). We document the oviposition, larval use and pupation of the Annonaceae specialised and geographically widespread Graphium eurypylus on a Magnoliaceae species, all under field conditions in Queensland, Australia. This is the first time such field observations of oviposition and larval feeding on Michelia champaca (Magnoliaceae) have been documented anywhere for this species.     

Genetic divergence, range expansion and possible homoploid hybrid speciation among pine species in Northeast China

Although homoploid hybrid speciation in plants is probably more common than previously realized, there are few well-documented cases of homoploid hybrid origin in conifers. We examined genetic divergence between two currently widespread pines in Northeast China, Pinus sylvestris var. mongolica and Pinus densiflora, and also whether two narrowly distributed pines in the same region, Pinus funebris and Pinus takahasii, might have originated from the two widespread species by homoploid hybrid speciation. Our results, based on population genetic analysis of chloroplast (cp), mitochondrial (mt) DNA, and nuclear gene sequence variation, showed that the two widespread species were divergent for both cp- and mtDNA variation, and also for haplotype variation at two of eight nuclear gene loci surveyed. Our analysis further indicated that P. sylvestris var. mongolica and P. densiflora remained allopatric during the most severe Quaternary glacial period that occurred in Northeast China, but subsequently exhibited rapid range expansions. P. funebris and P. takahasii, were found to contain a mixture of chlorotypes and nuclear haplotypes that distinguish P. sylvestris var. mongolica and P. densiflora, in support of the hypothesis that they possibly originated via homoploid hybrid speciation following secondary contact and hybridization between P. sylvestris var. mongolica and P. densiflora.     

The ecological genetics of homoploid hybrid speciation

Our understanding of homoploid hybrid speciation has advanced substantially since this mechanism of species formation was codified 50 years ago. Early theory and research focused almost exclusively on the importance of chromosomal rearrangements, but it later became evident that natural selection, specifically ecological selection, might play a major role as well. In light of this recent shift, we present an evaluation of ecology's role in homoploid hybrid speciation, with an emphasis on the genetics underlying ecological components of the speciation process. We briefly review new theoretical developments related to the ecology of homoploid hybrid speciation; propose a set of explicit, testable questions that must be answered to verify the role of ecological selection in homoploid hybrid speciation; discuss published work with reference to these questions; and also report new data supporting the importance of ecological selection in the origin of the homoploid hybrid sunflower species Helianthus deserticola. Overall, theory and empirical evidence gathered to date suggest that ecological selection is a major factor promoting homoploid hybrid speciation, with the strongest evidence coming from genetic studies.     

Historical demography of four gecko species specializing in boulder cave habitat: Implications in the evolutionary dead end hypothesis and conservation

Specialization in narrow ecological niches may not only help species to survive in competitive or unique environments but also contribute to their extermination over evolutionary time. Although the “evolutionary dead end” hypothesis has long been debated, empirical evidence from species with detailed information on niche specialization and evolutionary history remains rare. Here we use a group of four closely related Cnemaspis gecko species that depend highly on granite boulder caves in the Mekong Delta to investigate the potential impact of ecological specialization on their evolution and population dynamics. Isolated by unsuitable floodplain habitats, these boulder‐dwelling geckos are among the most narrowly distributed Squamata in the world. We applied several coalescence‐based approaches combined with the RAD‐seq technique to estimate their divergence times, gene flow and demographic fluctuations during the speciation and population differentiation processes. Our results reveal long‐term population shrinkage in the four geckos and limited gene flow during their divergence. The results suggest that the erosion and fragmentation of the granite boulder hills have greatly impacted population divergence and declines. The habitat specialization of these geckos has led to fine‐scaled speciation in these granite rocky hills; in contrast, specialization might also have pushed these species toward the edge of extinction. Our study also emphasizes the conservation urgency of these vulnerable, cave‐dependent geckos.     

Hitching a lift on the road to speciation

Understanding how speciation can take place in the presence of homogenizing gene flow remains a major challenge in evolutionary biology. In the early stages of ecological speciation, reproductive isolation between populations occupying different habitats is expected to be concentrated around genes for local adaptation. These genomic regions will show high divergence while gene exchange in other regions of the genome should continue relatively unimpaired, resulting in low levels of differentiation. The problem is to explain how speciation progresses from this point towards complete reproductive isolation, allowing genome‐wide divergence. A new study by Via and West (2008) on speciation between host races of the pea aphid, Acyrthosiphon pisum, introduces the mechanism of ‘divergence hitchhiking’ which can generate large ‘islands of differentiation’ and facilitate the build‐up of linkage disequilibrium, favouring increased reproductive isolation. This idea potentially removes a major stumbling block to speciation under continuous gene flow.     

ECOLOGICAL VERSUS PHYLOGENETIC DETERMINANTS OF TROPHIC ASSOCIATIONS IN A PLANT–LEAFMINER–PARASITOID FOOD WEB

Specialized trophic interactions in plant–herbivore–parasitoid food webs can spur “bottom–up” diversification if speciation in plants leads to host‐shift driven divergence in insect herbivores, and if the effect then cascades up to the third trophic level. Conversely, parasitoids that search for victims on certain plant taxa may trigger “top–down” diversification by pushing herbivores into “enemy‐free space” on novel hosts. We used phylogenetic regression methods to compare the relative importance of ecology versus phylogeny on associations between Heterarthrinae leafmining sawflies and their parasitoids. We found that: (1) the origin of leafmining led to escape from most parasitoids attacking external‐feeding sawflies; (2) the current enemies mainly consist of generalists that are shared with other leafmining taxa, and of more specialized lineages that may have diversified by shifting among heterarthrines; and (3) parasitoid–leafminer associations are influenced more by the phylogeny of the miners’ host plants than by relationships among miner species. Our results suggest that vertical diversifying forces have a significant—but not ubiquitous—role in speciation: many of the parasitoids have remained polyphagous despite niche diversification in the miners, and heterarthrine host shifts also seem to be strongly affected by host availability.     

Thinking in continua: beyond the “adaptive radiation” metaphor

“Adaptive radiation” is an evocative metaphor for explosive evolutionary divergence, which for over 100 years has given a powerful heuristic to countless scientists working on all types of organisms at all phylogenetic levels. However, success has come at the price of making “adaptive radiation” so vague that it can no longer reflect the detailed results yielded by powerful new phylogeny‐based techniques that quantify continuous adaptive radiation variables such as speciation rate, phylogenetic tree shape, and morphological diversity. Attempts to shoehorn the results of these techniques into categorical “adaptive radiation: yes/no” schemes lead to reification, in which arbitrary quantitative thresholds are regarded as real. Our account of the life cycle of metaphors in science suggests that it is time to exchange the spent metaphor for new concepts that better represent the full range of diversity, disparity, and speciation rate across all of life.     

Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: implications for the origin of Helianthus paradoxus,a diploid hybrid species

For a new diploid or homoploid hybrid species to become established, it must diverge ecologically from parental genotypes. Otherwise the hybrid neospecies will be overcome by gene flow or competition. We initiated a series of experiments designed to understand how the homoploid hybrid species, Helianthus paradoxus, was able to colonize salt marsh habitats, when both of its parental species (H. annuusxH. petiolaris) are salt sensitive. Here, we report on the results of a quantitative trait locus (QTL) analysis of mineral ion uptake traits and survivorship in 172 BC2 hybrids between H. annuus and H. petiolaris that were planted in H. paradoxus salt marsh habitat in New Mexico. A total of 14 QTLs were detected for mineral ion uptake traits and three for survivorship. Several mineral ion QTLs mapped to the same position as the survivorship QTLs, confirming previous studies, which indicated that salt tolerance in Helianthus is achieved through increased Ca uptake, coupled with greater exclusion of Na and related mineral ions. Of greater general significance was the observation that QTLs with effects in opposing directions were found for survivorship and for all mineral ion uptake traits with more than one detected QTL. This genetic architecture provides an ideal substrate for rapid ecological divergence in hybrid neospecies and offers a simple explanation for the colonization of salt marsh habitats by H. paradoxus. Finally, selection coefficients of +0.126, -0.084 and -0.094 for the three survivorship QTLs, respectively, are sufficiently large to account for establishment of new, homoploid hybrid species.     

ON THE COYNE AND ORR‐IGIN OF SPECIES: EFFECTS OF INTRINSIC POSTZYGOTIC ISOLATION,ECOLOGICAL DIFFERENTIATION,X CHROMOSOME SIZE,AND SYMPATRY ON DROSOPHILA SPECIATION

Coyne and Orr found that mating discrimination (premating isolation) evolves much faster between sympatric than allopatric Drosophila species pairs. Their meta‐analyses established that this pattern, expected under reinforcement, is common and that Haldane's rule is ubiquitous in Drosophila species divergence. We examine three possible contributors to the reinforcement pattern: intrinsic postzygotic isolation, dichotomized as to whether hybrid males show complete inviability/sterility; host‐plant divergence, as a surrogate for extrinsic postzygotic isolation; and X chromosome size, whether roughly 20% or 40% of the genome is X‐linked. We focus on “young” species pairs with overlapping ranges, contrasted with allopatric pairs. Using alternative criteria for “sympatry” and tests that compare either level of prezygotic isolation in sympatry or frequency of sympatry, we find no statistically significant effects associated with X chromosome size or our coarse quantifications of intrinsic postzygotic isolation or ecological differentiation. Although sympatric speciation seems very rare in animals, the pervasiveness of the reinforcement pattern and the commonness of range overlap for close relatives indicate that speciation in Drosophila is often not purely allopatric. It remains to determine whether increased premating isolation with sympatry results from secondary contact versus parapatric speciation and what drives this pattern.