Host Conservatism Research Articles

Evolution of host use in fungivorous ciid beetles (Coleoptera: Ciidae): Molecular phylogeny focusing on Japanese taxa

Consumer–resource interactions between trophic levels are ubiquitous and important factors in shaping the diversity of insects. However, dietary patterns such as host specificity and conservatism have been insufficiently examined in fungivorous insects. Here we reconstructed the evolutionary history of host use in fungivorous ciid beetles (Coleoptera: Ciidae) and tested for host conservatism. Phylogenetic relationships among 49 species from Japan were inferred by using a large sequence data set from ultraconserved elements (UCEs). In addition, sequences of three genes (COI, 28S rRNA, 18S rRNA) were analyzed to reconstruct the phylogeny for 130 OTUs from a broader range of taxa and geographic regions using the UCE tree as a backbone topology. We found that Ciini and Orophiini are not recovered as reciprocally monophyletic groups. As previously suggested, the largest genus Cis Latreille was also not monophyletic. Ancestral-state reconstruction of host use in both datasets showed that Ciidae species were clustered by host-use group across the tree. This pattern was confirmed by the significantly lower transition rate compared with expectations under the random shift hypothesis. The observed conservatism in host use implied these beetles possess unique adaptations to specific fungal taxa, just as herbivorous insects are adapted to specific plant taxa.

Biodiversity, Evolution and Ecological Specialization of Baculoviruses: A Treasure Trove for Future Applied Research.

The Baculoviridae, a family of insect-specific large DNA viruses, is widely used in both biotechnology and biological control. Its applied value stems from millions of years of evolution influenced by interactions with their hosts and the environment. To understand how ecological interactions have shaped baculovirus diversification, we reconstructed a robust molecular phylogeny using 217 complete genomes and ~580 isolates for which at least one of four lepidopteran core genes was available. We then used a phylogenetic-concept-based approach (mPTP) to delimit 165 baculovirus species, including 38 species derived from new genetic data. Phylogenetic optimization of ecological characters revealed a general pattern of host conservatism punctuated by occasional shifts between closely related hosts and major shifts between lepidopteran superfamilies. Moreover, we found significant phylogenetic conservatism between baculoviruses and the type of plant growth (woody or herbaceous) associated with their insect hosts. In addition, we found that colonization of new ecological niches sometimes led to viral radiation. These macroevolutionary patterns show that besides selection during the infection process, baculovirus diversification was influenced by tritrophic interactions, explained by their persistence on plants and interactions in the midgut during horizontal transmission. This complete eco-evolutionary framework highlights the potential innovations that could still be harnessed from the diversity of baculoviruses.

Host conservatism, geography, and elevation in the evolution of a Neotropical moth radiation.

The origins of evolutionary radiations are often traced to the colonization of novel adaptive zones, including unoccupied habitats or unutilized resources. For herbivorous insects, the predominant mechanism of diversification is typically assumed to be a shift onto a novel lineage of host plants. However, other drivers of diversification are important in shaping evolutionary history, especially for groups residing in regions with complex geological histories. We evaluated the contributions of shifts in host plant clade, bioregion, and elevation to diversification in Eois (Lepidoptera: Geometridae), a hyper-diverse genus of moths found throughout the Neotropics. Relationships among 107 taxa were reconstructed using one mitochondrial and two nuclear genes. In addition, we used a genotyping-by-sequencing approach to generate 4641 SNPs for 137 taxa. Both datasets yielded similar phylogenetic histories, with relationships structured by host plant clade, bioregion, and elevation. While diversification of basal lineages often coincided with host clade shifts, more recent speciation events were more typically associated with shifts across bioregions or elevational gradients. Overall, patterns of diversification in Eois are consistent with the perspective that shifts across multiple adaptive zones synergistically drive diversification in hyper-diverse lineages.

Two recently discovered species of Apiomorpha (Hemiptera: Eriococcidae) feeding on eudesmid eucalypts in Western Australia reaffirm host conservatism in this gall-inducing scale insect genus

Gall-inducing insects are relatively host-specific compared with their non-galling relatives. In Australia, there have been at least four origins of gall induction among eriococcid scale insects, with the most species-rich genus, Apiomorpha, inducing galls only on species of Eucalyptus. Here we describe two recently discovered species of Apiomorpha that induce galls on eudesmid eucalypts in Western Australia: Apiomorpha gongylocarpae, sp. nov., which is very similar morphologically to A. pomaphora, and A. jucundacrispi, sp. nov., the adult females of which induce an unusual gall covered in woody protrusions that, when older, have a knobbly appearance. Using molecular, morphological and host-association data, we show that these two species form a monophyletic group with the only other species of Apiomorpha that feed on eudesmid eucalypts (A. hilli and A. pomaphora). We place all four species of eudesmid-feeding Apiomorpha in the A. hilli species group, thus revising the current placement of A. pomaphora by removing it from the A. malleeacola species group. This study highlights additional faunal diversity endemic to Western Australia, with two of the four species being restricted to the globally recognised biodiversity hotspot of the South West Australia Floristic Region. http://zoobank.org/urn:lsid:zoobank.org:pub:D6245EB6-903E-483C-B69B-3ED7EA35AD04.

Phylogenetic congruence of parasitic smut fungi (Anthracoidea, Anthracoideaceae) and their host plants (Carex, Cyperaceae): Cospeciation or host-shift speciation?

• Fahrenholz's rule states that common ancestors of extant parasites were parasites of the common ancestors of extant hosts. Consequently, parasite phylogeny should mirror host phylogeny. The smut fungi genus Anthracoidea (Anthracoideaceae) is mainly hosted by species of the genus Carex (Cyperaceae). Whether smut fungi phylogeny mirrors sedge phylogeny is still under debate.• The nuclear large subunit DNA region (LSU; 57 accessions) from 31 Anthracoidea species and the ITS, ETS, and trnL-F spacer-trnL intron complex from 41 Carex species were used to infer the phylogenetic history of parasites and their hosts using a maximum likelihood approach. Event-based and distance-based cophylogenetic methods were used to test the hypothesis of whether the phylogeny of smut fungi from the genus Anthracoidea matches the phylogeny of the sedge Carex species they host.• Cophylogenetic reconstructions taking into account phylogenetic uncertainties based on event-based analyses demonstrated that the Anthracoidea phylogeny has significant topological congruence with the phylogeny of their Carex hosts. A distance-based test was also significant; therefore, the phylogenies of Anthracoide and Carex are partially congruent.• The phylogenetic congruence of Anthracoidea and Carex is partially based on smut fungi species being preferentially hosted by closely related sedges (host conservatism). In addition, many different events rather than only codivergence events are inferred. All of this evidence suggests that host-shift speciation rather than cospeciation seems to explain the cophylogenetic patterns of Anthracoidea and Carex.

Ectomycorrhizal fungal communities on the endangered Chinese Douglas-fir (Pseudotsuga sinensis) indicating regional fungal sharing overrides host conservatism across geographical regions

Background and aims Ectomycorrhizal (ECM) fungal communities are affected by many abiotic and biotic factors, among which host identity is often regarded as the most significant. Although little about ECM fungal communities on endangered tree species is known, knowledge of their ECM associations could be a key to conservation given the functional importance of the symbiosis.

Host conservatism or host specialization? Patterns of fungal diversification are influenced by host plant specificity inOphiognomonia(Gnomoniaceae: Diaporthales)

In this study evolutionary host plant patterns at ranks from order to species were analysed using spatial evolutionary and ecological vicariance analysis (SEEVA), based on a multigene phylogeny of 45 ascomycete fungal species. The objective was to understand speciation events and host associations in Ophiognomonia (Gnomoniaceae). Species of this genus are perithecial fungi that occur as endophytes, pathogens, and latent saprobes on plants in the families of Betulaceae, Fagaceae, Juglandaceae, Lauraceae, Malvaceae, Platanaceae, Rosaceae, Salicaceae, and Sapindaceae. A second objective was to determine whether speciation events are influenced by host conservatism, host specialization, or host switching at different taxonomic host ranks. Host differences between sister clades were interpreted using the divergence index (D) from the SEEVA analysis, ranging from 0 for no divergence to 1 for maximum possible divergence. Several fungal subclades showed clear patterns of host order/family conservatism (D = 1.00) for hosts in Betulaceae, Fagaceae, Juglandaceae, and Rosaceae. Clear trends of host specialization at host genus and species ranks (D = 1.00) were suggested within these host families. Independent host jumps were observed for two species at the family rank and three at the order rank. As a result of this study, host specificity and specialization is hypothesized as a mechanism that can strongly contribute to speciation patterns in fungal pathogens. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 1–16.

Ancient host shifts followed by host conservatism in a group of ant parasitoids

While ant colonies serve as host to a diverse array of myrmecophiles, few parasitoids are able to exploit this vast resource. A notable exception is the wasp family Eucharitidae, which is the only family of insects known to exclusively parasitize ants. Worldwide, approximately 700 Eucharitidae species attack five subfamilies across the ant phylogeny. Our goal is to uncover the pattern of eucharitid diversification, including timing of key evolutionary events, biogeographic patterns and potential cophylogeny with ant hosts. We present the most comprehensive molecular phylogeny of Eucharitidae to date, including 44 of the 53 genera and fossil-calibrated estimates of divergence dates. Eucharitidae arose approximately 50 Ma after their hosts, during the time when the major ant lineages were already established and diversifying. We incorporate host association data to test for congruence between eucharitid and ant phylogenies and find that their evolutionary histories are more similar than expected at random. After a series of initial host shifts, clades within Eucharitidae maintained their host affinity. Even after multiple dispersal events to the New World and extensive speciation within biogeographic regions, eucharitids remain parasitic on the same ant subfamilies as their Old World relatives, suggesting host conservatism despite access to a diverse novel ant fauna.

Delayed colonisation of Acacia by thrips and the timing of host-conservatism and behavioural specialisation.

BackgroundRepeated colonisation of novel host-plants is believed to be an essential component of the evolutionary success of phytophagous insects. The relative timing between the origin of an insect lineage and the plant clade they eat or reproduce on is important for understanding how host-range expansion can lead to resource specialisation and speciation. Path and stepping-stone sampling are used in a Bayesian approach to test divergence timing between the origin of Acacia and colonisation by thrips. The evolution of host-plant conservatism and ecological specialisation is discussed.ResultsResults indicated very strong support for a model describing the origin of the common ancestor of Acacia thrips subsequent to that of Acacia. A current estimate puts the origin of Acacia at approximately 6 million years before the common ancestor of Acacia thrips, and 15 million years before the origin of a gall-inducing clade. The evolution of host conservatism and resource specialisation resulted in a phylogenetically under-dispersed pattern of host-use by several thrips lineages.ConclusionsThrips colonised a diversity of Acacia species over a protracted period as Australia experienced aridification. Host conservatism evolved on phenotypically and environmentally suitable host lineages. Ecological specialisation resulted from habitat selection and selection on thrips behavior that promoted primary and secondary host associations. These findings suggest that delayed and repeated colonisation is characterised by cycles of oligo- or poly-phagy. This results in a cumulation of lineages that each evolve host conservatism on different and potentially transient host-related traits, and facilitates both ecological and resource specialisation.

The global phylogeny of the subfamily Sycoryctinae (Pteromalidae): Parasites of an obligate mutualism

The inflorescences of fig trees (Ficus, Moraceae) host well-defined, host plant specific wasp communities that lend themselves to tests of hypotheses on insect diversification. We provide the first estimate of the global molecular phylogeny for the Sycoryctinae – a large subfamily of fig wasps consisting mainly of parasitoids of fig-pollinating wasps. We find strong support for a large Old World clade that contains eight of the eleven genera, in the tribes Sycoryctini and Philotrypesini. The sister taxon is tribe Apocryptini, comprising the genera Apocrypta and Bouceka. Finally, a new tribe, Critogastrini, is raised for the genus Critogaster, sister to all other sycoryctines. At the genus level, we found a general pattern of strong host conservatism, in which closely related wasps associate with closely related figs. Despite this, there is also evidence for multiple host shifts between more distantly related figs in some wasp genera (especially Philotrypesis). We estimate Sycoryctinae to have originated 49–64Ma, after the initial co-radiation of the host figs and pollinators. Further, conservative assumptions in our analyses probably overestimate the age of the sycoryctines. Together, patterns of host association, evidence for a mix of host constraints and host shifting, and molecular dating suggest that sycoryctine parasites radiated through delayed phylogenetic tracking of their hosts. This contributes to the growing body of literature suggesting that coevolving parasites often radiate after their hosts.

Phylogenetics and evolution of host-plant use in leaf-mining sawflies (Hymenoptera: Tenthredinidae: Heterarthrinae)

The habit of mining within leaves has evolved convergently in numerous plant-feeding insect taxa. Many leaf-mining groups contain a large number of species with distinct feeding preferences, which makes them highly suitable for studies on the evolutionary history of host-plant use and on the role of niche shifts in speciation. We aimed to clarify the origin, classification, and ecological evolution of the tenthredinid sawfly subfamily Heterarthrinae, which contains c. 150 leaf-mining species that collectively feed on over 20 plant genera around the world. For this, we reconstructed the phylogeny of representative heterarthrine species and diverse outgroups from the superfamily Tenthredinoidea on the basis of DNA sequence data collected from two mitochondrial (CoI and Cytb) and two nuclear (EF-1α and NaK) genes. Thereafter, we inferred the history of niche diversification within Heterarthrinae by plotting larval host-plant associations on the trees, and by contrasting a time-calibrated leaf-miner phylogeny with the phylogeny of their host plants. The results show that: (1) heterarthrine leaf-miners constitute a monophyletic group that arose from external-feeding blennocampine lineages within the Tenthredinidae c. 110–80 million years ago; (2) heterarthrines generally radiated well after their host taxa, and extant host-plant associations therefore result from a combination of host conservatism and occasional shifts among available plant taxa; and (3) diversification in Heterarthrinae apparently occurs by multiple mechanisms, including sympatric or allopatric ecological speciation, non-ecological allopatric speciation, and possibly allochronic speciation. Overall, both present and historical host-use patterns within the Heterarthrinae exhibit striking similarities to patterns found in co-occurring herbivore taxa.

Host conservatism, host shifts and diversification across three trophic levels in two Neotropical forests

Host-parasite systems have been models for understanding the connection between shifts in resource use and diversification. Despite theoretical expectations, ambiguity remains regarding the frequency and importance of host switches as drivers of speciation in herbivorous insects and their parasitoids. We examine phylogenetic patterns with multiple genetic markers across three trophic levels using a diverse lineage of geometrid moths (Eois), specialist braconid parasitoids (Parapanteles) and plants in the genus Piper. Host-parasite associations are mapped onto phylogenies, and levels of cospeciation are assessed. We find nonrandom patterns of host use within both the moth and wasp phylogenies. The moth-plant associations in particular are characterized by small radiations of moths associated with unique host plants in the same geographic area (i.e. closely related moths using the same host plant species). We suggest a model of diversification that emphasizes an interplay of factors including host shifts, vicariance and adaptation to intraspecific variation within hosts.

Molecular Divergence in AllopatricCeratosolen(Agaonidae) Pollinators of Geographically WidespreadFicus(Moraceae) Species

AbstractSpeciation in pollinating seed predators such as fig wasps (Hymenoptera: Agaonidae) is likely to have been influenced by a combination of ecological and geographical isolating mechanisms, but recent molecular analyses of fig wasps have focused on pollinator specialization as the main factor driving speciation. This study investigates the contribution of geographic modes of speciation such as dispersal, vicariance, and isolation by distance. We sampled haplotypes of mitochondrial cytochrome oxidase I from Ceratosolen pollinators of six geographically widespread Australasian fig (Moraceae: Ficus) species, including four species spanning Wallacea. Phylogenetic analysis investigated the extent of host conservatism and host switching accompanying divergence in Ceratosolen. Geographically widespread Ceratosolen showed deep intraspecific divergence exceeding or comparable to divergence between named sister species. Maximum parsimony and Bayesian analyses supported species monophyly in five of six cases, whereas results for a sixth species were equivocal. Bayesian divergence time estimation suggested dispersal across Wallacea during the Miocene epoch, after the collision of Australian and Asian continental plates. Cryptic species were evident in all six focal taxa. Because the deep mitochondrial divergence within these taxa is regionally distributed, allopatric divergence provides a simple explanation for the existence of these cryptic lineages pollinating widespread fig species. We found little evidence of divergence accompanied by host switching. The ancient origin of cryptic and geographically isolated species suggests that long-distance dispersal may be rare in Ceratosolen and that host associations are generally conserved during range expansion.

Evolution of host utilization patterns in the seed beetle genus Mimosestes Bridwell (Coleoptera: Chrysomelidae: Bruchinae)

The evolutionary history of diet breadth expansion and intergeneric host shifts in the seed beetle genus Mimosestes were reconstructed to investigate the process of host range expansion in phytophagous insects. The evolutionary correlation between diet breadth and variation in oviposition behavior of Mimosestes was also examined to estimate the process of generalist evolution within the genus. Ancestral state reconstruction based on a molecular phylogeny inferred from three mitochondrial markers (16S rRNA, 12S rRNA, and COI) and one nuclear marker (EF-1α) revealed that host utilization patterns were shaped by repeated colonizations to novel or pre-adapted host plants. Neither plant genus and species group level host conservatism nor an evolutionary tendency toward specialization was found in the genus, contrary to the expectations of plant–insect co-evolutionary theory. In addition, statistical analyses revealed that diet breadth was significantly correlated with oviposition behavior, suggesting that behavioral factors such as the oviposition preferences of female seed beetles affect the expansion of diet breadth in generalists.

Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands

The degree to which haematozoan parasites can exploit a range of vectors and hosts has both ecological and evolutionary implications for their transmission and biogeography. Here we explore the extent to which closely related mosquito species share the same or closely related haematozoan parasites, and examine the overlap in parasite lineages with those isolated from avian hosts, Zosterops species, sampled across the same study sites. Mosquito samples were collected and analysed (14 species, n = 804) from four islands in Vanuatu and the main island of New Caledonia. Using polymerase chain reaction, 15.5% (14/90) of pooled mosquito (thoracic) samples showed positive amplifications. Subsequent phylogenetic analysis of the cytochrome b gene identified four genetically distinct Plasmodium and two Haemoproteus lineages from these samples, five of which were identical to parasite lineages (n = 21) retrieved from the avian hosts. We found that three Plasmodium lineages differing by a maximum of 0.9% sequence divergence were recovered from different species and genera of mosquitoes and two Haemoproteus lineages differing by 4.6% sequence divergence were carried by 10 distantly related (11-21% divergent) mosquito species. These data suggest a lack of both cospeciation and invertebrate host conservatism. Without experimental demonstration of the transmission cycle, it is not possible to establish whether these mosquitoes are the biological vectors of isolated parasite lineages, reflecting a limitation of a purely polymerase chain reaction-based approach. Nonetheless, our results raise the possibility of a new transmission pathway and highlight extensive invertebrate host shifts in an insular mosquito-parasite system.

Specialized host‐plant performance of the cotton aphid is altered by experience

AbstractAlthough distinct host specialization is observed for the cotton‐melon aphid (Aphis gossypii Glover) on cotton and cucurbit plants, it is still ambiguous whether the specialization is altered by experience on a novel host plant. Here the performance of cotton and cucurbit‐specialized aphids, A. gossypii on novel host plants was studied by a host‐selection test and by the life‐table method. The two host‐specialized aphids cannot survive and establish populations after reciprocal host transfers. They have ability to recognize the host plants on which they were reared, and escape behavior from novel hosts was observed. Interestingly, the cotton and cucurbit‐specialized aphids survive and reproduce normally on hibiscus (Hibiscus syriacus), a main overwintering host plant, and host‐fidelity of A. gossypii to cucurbit plants is altered by feeding and living experience on hibiscus, which confers the same capacity to use cotton and cucumber on to the cucurbit‐specialized population, but host‐fidelity to cotton is not altered and the fitness of the cotton specialized population to cucumber is still poorer. A. gossypii from hibiscus has a significant preference for cotton to cucumber in the host‐selection process, and none stays on cucumber more than 20 h after transfer. The results presented imply that cucurbit‐specialized aphids might not return to an overwintering host plant (hibiscus) in wild fields, so host conservatism to cucurbit plants is maintained. The potential of cucurbit‐specialized aphids of A. gossypii to use cotton plants, intermediated by experience on hibiscus, suggests that the specialized host‐plant performance of phytophagous insects is not wholly conservative.

Dietary specialization in European species groups of seed beetles (Coleoptera: Bruchidae: Bruchinae)

Because of their particular biology, seed beetles exhibit a strong relationship with their larval host plants. In Europe, however, field data have long been scarce and unreliable. The results of Legume seed collections of nearly 1,000 samples belonging to 292 species from various locations in Europe are summarized. The status of current Bruchidius species groups is amended on morphological and phylogenetic bases. Recent advances in the knowledge of phylogenetic structures of both Fabaceae and Bruchinae provide a new picture of Bruchinae-Fabaceae interactions. It reveals a certain level of host conservatism. The hypothesis of radiative adaptation seems the most compatible with observed data.

Phylogenetic Relationships of Fig Wasps Pollinating Functionally Dioecious Ficus Based on Mitochondrial DNA Sequences and Morphology

The obligate mutualism between pollinating fig wasps in the family Agaonidae (Hymenoptera: Chalcidoidea) and Ficus species (Moraceae) is often regarded as an example of co-evolution but little is known about the history of the interaction, and understanding the origin of functionally dioecious fig pollination has been especially difficult. The phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus were inferred from mitochondrial cytochrome oxidase gene sequences (mtDNA) and morphology. Separate and combined analyses indicated that the pollinators of functionally dioecious figs are not monophyletic. However, pollinator relationships were generally congruent with host phylogeny and support a revised classification of Ficus. Ancestral changes in pollinator ovipositor length also correlated with changes in fig breeding systems. In particular, the relative elongation of the ovipositor was associated with the repeated loss of functionally dioecious pollination. The concerted evolution of interacting morphologies may bias estimates of phylogeny based on female head characters, but homoplasy is not so strong in other morphological traits. The lesser phylogenetic utility of morphology than of mtDNA is not due to rampant convergence in morphology but rather to the greater number of potentially informative characters in DNA sequence data; patterns of nucleotide substitution also limit the utility of mtDNA findings. Nonetheless, inferring the ancestral associations of fig pollinators from the best-supported phylogeny provided strong evidence of host conservatism in this highly specialized mutualism.

A HISTORY OF HOST ASSOCIATIONS AND EVOLUTIONARY DIVERSIFICATION FOR OPHRAELLA (COLEOPTERA: CHRYSOMELIDAE): NEW EVIDENCE FROM MITOCHONDRIAL DNA.

A rapidly growing supply of phylogenetic trees has fueled a burst of insights into the ways that phylogenetic data might inform our study of evolution (e.g., Lauder 1990; Wanntorp et al. 1990; Brooks and McLennan 1991; Harvey and Pagel 1991; Swofford and Maddison 1992). One area in which these approaches have proven particularly useful is the study of coevolution (Mitter and Brooks 1983; Brooks 1988; Miller 1991; Mitter et al. 1991; Brooks and McLennan 1993), the cladogenetic and selective influences that ecologically coupled taxa exert on each other through evolutionary time. Those who study the coevolution of herbivorous insects and their host plants have repeatedly noted both the relative host specificity of most herbivore species and the taxonomic conservatism that often characterizes the host affiliations of insect genera and families (Dethier 1954; Ehrlich and Raven 1964; Ward and Spalding 1993). Certain explanations for these patterns can be tested phylogenetically. For example, if herbivore lineages remain strictly associated with their host species over sufficient periods of evolutionary time, vicariance events that isolate populations of the host will also isolate populations of the herbivore. To the extent that these events lead to the formation of new species, this combination of host loyalty and parallel cladogenesis (Benson et al. 1975; Mitter and Brooks 1983; Spencer 1988) can account for both host specificity and host conservatism. If this allopatric cospeciation scenario (Brooks 1979) holds, the phylogenies of host plant taxa and their insect parasites will be at least roughly concordant. Topological contradictions between these trees, however, suggest that herbivore lineages have switched their affinities from one plant group to another subsequent to the diversification of these plants (Jermy 1984; Brooks 1988). To date, most of the handful of pertinent studies (reviewed in Mitter and Farrell 1991) have found evidence for such host shifts, but a few notable exceptions are strongly consistent with the cospeciation model (Farrell and Mitter 1990; B. Farrell in prep.). But if host shifts commonly occur, why do they involve the particular (and often related) plant species that they do, given that selection pressures favoring the use of locally common nonhosts must be omnipresent (Futuyma 1983)? Such conservatism suggests that the spectrum of likely host shifts may be limited by constraints on adaptively relevant genetic variation, perhaps because of the host associations of an her-