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.     

Comprehensive gene and taxon coverage elucidates radiation patterns in moths and butterflies

Lepidoptera (butterflies and moths) represent one of the most diverse animals groups. Yet, the phylogeny of advanced ditrysian Lepidoptera, accounting for about 99 per cent of lepidopteran species, has remained largely unresolved. We report a rigorous and comprehensive analysis of lepidopteran affinities. We performed phylogenetic analyses of 350 taxa representing nearly 90 per cent of lepidopteran families. We found Ditrysia to be a monophyletic taxon with the clade Tischerioidea + Palaephatoidea being the sister group of it. No support for the monophyly of the proposed major internested ditrysian clades, Apoditrysia, Obtectomera and Macrolepidoptera, was found as currently defined, but each of these is supported with some modification. The monophyly or near-monophyly of most previously identified lepidopteran superfamilies is reinforced, but several species-rich superfamilies were found to be para- or polyphyletic. Butterflies were found to be more closely related to ‘microlepidopteran’ groups of moths rather than the clade Macrolepidoptera, where they have traditionally been placed. There is support for the monophyly of Macrolepidoptera when butterflies and Calliduloidea are excluded. The data suggest that the generally short diverging nodes between major groupings in basal non-tineoid Ditrysia are owing to their rapid radiation, presumably in correlation with the radiation of flowering plants.     

Molecular phylogeny of Eois (Lepidoptera,Geometridae): evolution of wing patterns and host plant use in a species‐rich group of Neotropical moths

Strutzenberger, P., Brehm, G., Bodner, F. & Fiedler K. (2010). Molecular phylogeny of Eois (Lepidoptera, Geometridae): evolution of wing patterns and host plant use in a species‐rich group of Neotropical moths. —Zoologica Scripta, 39, 603–620. Eois is a pantropical genus of Geometridae moths with currently 250 valid described species, the majority of which occur in the Neotropics. Eois is a prominent component of Andean moth communities locally accounting for up to ～10% of geometrid individuals. We address the evolution of wing patterns and host plant use in Neotropical Eois and provide a preliminary assessment on the monophyly and biogeographic history of the entire genus as well as affinities within the subfamily Larentiinae. We applied Bayesian, maximum likelihood and maximum parsimony methods of phylogenetic reconstruction to a 142 taxon dataset of partial COI (1220 bp) and Ef1α (1066 bp) sequences resulting in the largest taxon set of geometrid moths analyzed in a molecular phylogenetic study so far. Monophyly of Eois was always strongly supported. Ten monophyletic clades were found with good support, seven of which have characteristic wing pattern phenotypes. Only one wing pattern type occurs in two clades. Trophic associations with representatives of the family Piperaceae occur in all 8 (of 9) Neotropical clades for which host information is available. Apart from feeding on Piper, at least two Eois species in Ecuador feed on Peperomia, and one on Manekia (all Piperaceae); two further species live on Hedyosmum (Chloranthaceae). Species feeding on Peperomia, Manekia and Hedyosmum are usually nested in Piper‐associated clades. Single records of associations with Gesneriaceae and Monimiaceae are scattered in otherwise Piperaceae‐associated clades. These patterns suggest multiple parallel host shifts away from Piper as ancestral food plant. Old World Eois were recovered as monophylum and sister to Neotropical Eois. Within the subfamily Larentiinae the genus Eois has previously been placed close to the tribe Eupitheciini, but this was not supported in our phylogenetic analyses.     

Plant odour processing in the antennal lobe of male and female grapevine moths,Lobesia botrana (Lepidoptera: Tortricidae)

Moths of Lobesia botrana (Lepidoptera: Tortricidae) are confronted with different volatiles emitted from the host plant during the different seasons. To test the hypothesis of plasticity of central plant odour processing in moths of different generations in the future, we first investigated the responses of antennal lobe (AL) interneurons of laboratory-reared virgin and mated males and females. We used intracellular recording and staining techniques while stimulating the antenna with a range of host and non-host plant odours. The AL structure of L. botrana is similar to that found in other Lepidoptera species studied. The most frequent physiological responses for all types of moths were obtained with (E)-2-hexenal, and with thujyl alcohol and β-thujone, components of tansy, a behaviourally attractive non-host plant. Some broadly responding neurons were capable of distinguishing between different compounds through different response patterns (excitation/inhibition) and/or different dose-response characteristics. Response characteristics (response spectra, threshold and specificity) of neurons were similar, independent of sex or mating status of the moths. Significant differences between the groups were, however, found in the proportion of responding neurons for a few tested components.     

Phylogenetic diversity of geometrid moths decreases with elevation in the tropical Andes

Species diversity of geometrid moths (Lepidoptera, Geometridae) has previously been shown to be extremely and constantly high along a continuously forested elevational gradient in the Andes of southern Ecuador. We analysed samples taken from 32 sites between 1999 and 2011 in northern Podocarpus National Park and adjacent areas from 1020 to 2916 m a.s.l. We conjecture that high elevation habitats were historically mostly colonised by species from lower elevations, and that environmental filtering (e.g. through host plant specificity or temperature tolerance) constrained colonisation from lower elevations, which would yield a pattern of elevationally decreasing phylogenetic diversity. We analysed elevational phylogenetic patterns by means of: 1) the nearest‐taxon index (NTI), 2) DNA barcode‐based terminal branch lengths (TBLs) from maximum‐likelihood phylogeny, 3) the subfamily composition of the local assemblages, and 4), the rarefied number of morphologically defined genera per site. We counted a total of 1445 species. NTI values significantly increased with elevation, both in a conventional and a rarefaction approach. TBLs decreased significantly with elevation. Subfamily composition profoundly changed with elevation, particularly expressed as an increased proportion of the subfamily Larentiinae and decreased fractions of Sterrhinae and Geometrinae. The number of genera in equally rarefied species resamples significantly decreased with elevation. We conclude that environmental filtering indeed contributed to an altitudinal decrease in moth phylodiversity, but these constraints prevented only relatively few clades from colonising high elevation habitats.     

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.     

Diel behavior in moths and butterflies: a synthesis of data illuminates the evolution of temporal activity

Lepidoptera (butterflies and moths) are one of the most taxonomically diverse insect orders with nearly 160,000 described species. They have been studied extensively for centuries and are found on nearly all continents and in many environments. It is often assumed that adult butterflies are strictly diurnal and adult moths are strictly nocturnal, but there are many exceptions. Despite the broad interest in butterflies and moths, a comprehensive review of diel (day-night) activity has not been conducted. Here, we synthesize existing data on diel activity in Lepidoptera, trace its evolutionary history on a phylogeny, and show where gaps lie in our knowledge. Diurnality was likely the ancestral condition in Lepidoptera, the ancestral heteroneuran was likely nocturnal, and more than 40 transitions to diurnality subsequently occurred. Using species diversity estimates across the order, we predict that roughly 75-85% of Lepidoptera are nocturnal. We also define the three frequently used terms for activity in animals (diurnal, nocturnal, crepuscular), and show that literature on the activity of micro-moths is significantly lacking. Ecological factors leading to nocturnality/diurnality is a compelling area of research and should be the focus of future studies.     

Evaluation of pheromone-baited traps for winter moth and Bruce spanworm (Lepidoptera: Geometridae)

We tested different pheromone-baited traps for surveying winter moth, Operophtera brumata (L.) (Lepidoptera: Geometridae), populations in eastern North America. We compared male catch at Pherocon 1C sticky traps with various large capacity traps and showed that Universal Moth traps with white bottoms caught more winter moths than any other trap type. We ran the experiment on Cape Cod, MA, where we caught only winter moth, and in western Massachusetts, where we caught only Bruce spanworm, Operophtera bruceata (Hulst) (Lepidoptera: Geometridae), a congener of winter moth native to North America that uses the same pheromone compound [(Z,Z,Z)-1,3,6,9-nonadecatetraene] and is difficult to distinguish from adult male winter moths. With Bruce spanworm, the Pherocon 1C sticky traps caught by far the most moths. We tested an isomer of the pheromone [(E,Z,Z)-1,3,6,9-nonadecatetraene] that previous work had suggested would inhibit captures of Bruce spanworm but not winter moths. We found that the different doses and placements of the isomer suppressed captures of both species to a similar degree. We are thus doubtful that we can use the isomer to trap winter moths without also catching Bruce spanworm. Pheromone-baited survey traps will catch both species.     

Evolutionary history of the burnet moth genus Zygaena Fabricius, 1775 (Lepidoptera: Zygaenidae) inferred from nuclear and mitochondrial sequence data: phylogeny, host–plant association, wing pattern evolution and historical biogeography

Burnet moths of the genus Zygaena are a striking group of primarily diurnal Lepidoptera displaying an exceptional phenotypic plasticity. Previous attempts to elucidate the phylogenetic history of the group had been confounded by a perplexing pattern of characters or insufficient taxon sampling. In the present study, we infer a phylogeny of the genus Zygaena by analysing 5.4 kb of their nuclear and mitochondrial DNA. Eighty‐four of the 98 currently recognized species in this genus are considered, including representatives of all described species groups. RNA coding sequences are aligned with reference to zygaenoid moth specific secondary structure models of corresponding molecules. We conduct phylogenetic analyses within a Bayesian framework applying partition specific substitution parameters; covariation of paired sites in RNA gene sequences is accommodated by using doublet substitution models. The molecular data reveal that a considerable number of currently recognized species groups in Zygaena are not monophyletic. The traditional subgeneric classification proves to be artificial as well; Agrumenia and Zygaena (sensu stricto) are polyphyletic. Only the subgenus Mesembrynus can be confirmed as a monophyletic species cluster. Optimization of larval host–plant associations and forewing patterns on sampled trees of the Bayesian analyses suggest convergent evolution of similar wing pattern types in distantly related species clusters and a shift from cyanogenic to acyanogenic host‐plants. The phylogenetic results challenge the classic assumption that early species diversification in Zygaena took place in the Irano–Turkestanian region. Rather, the molecular data point to the western Mediterranean area as the geographical origin of the group and imply a subsequent colonization of the Middle East and Central Asia. We discuss the apparently convergent evolution of similar wing patterns in context with the chemical defence system of burnet moths and suggest a species group concept for the genus Zygaena that accounts for the recent findings. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92 , 501–520.     

Species traits predict island occupancy in noctuid moths

Knowing how species’ traits relate to processes that underlie occupancy patterns such as colonisation and population persistence, is important for our understanding of how species survive in fragmented and changing landscapes. We used automatic UV light-traps to sample noctuid moths on two remote islands, and compared traits of island occupants with those of a species pool from mainland southeast Sweden. Widely distributed species, generalist species, species with a long adult activity period and species active late in the summer had higher probability of occupancy on the remote islands. The results were consistent between islands. The traits of host plant specificity and species with an adult activity period during late summer remained robust and were statistically significant after controlling for any possible phylogenetic bias. This indicates that species exhibiting those traits survive better when habitat and climate changes. It is crucial to include our results in; (1) conservation planning, e.g. when devising conservation measures in fragmented landscapes; (2) for predictions of future occupancy patterns; and (3) ecosystem impact assessments, e.g. the importance of moths as pollinators, herbivores and being the functional link between parasitoids, plants, consumers and predators.     

Male courtship ultrasound produced by mesothoracic tymbal organs in the yellow peach moth <Emphasis Type="Italic">Conogethes punctiferalis</Emphasis> (Lepidoptera: Crambidae)

Insect sound-producing apparatuses are mostly classified into two types: file–scraper and tymbal. Structures and locations of these organs are conserved in some phylogenetic groups, e.g., crickets, grasshoppers, and cicadas. However, moths have evolved diversified sound-producing organs, such as wing castanets and proboscis, in addition to the file–scraper and tymbal, in each species. Here we demonstrate that the yellow peach moth Conogethes punctiferalis (Guenée) (Lepidoptera: Crambidae) has developed mesothoracic tymbal organs never reported so far in insects. Tymbals are male specific and used for generating ultrasonic clicks in mating. We found eight to nine striae on the smooth surface of the tymbal membrane, suggesting the production of several clicks by a single buckle of the membrane in association with contraction/relaxation of the mesothoracic muscles. Acoustic data from click sequences support the idea that the series is generated by side-to-side asynchrony with an active/passive half cycle by an inward/outward buckle, and thus in click group (pulse) production, males emit 28 clicks with the right and left tymbals. The click-producing mechanism is similar, but not homologous, to those of other clicking species in five moth families. Thus, moths have acquired tymbal organs through independent and convergent evolution.     

Morphological complexity affects the diversity of marine microbiomes

Large eukaryotes support diverse communities of microbes on their surface—epibiota—that profoundly influence their biology. Alternate factors known to structure complex patterns of microbial diversity—host evolutionary history and ecology, environmental conditions and stochasticity—do not act independently and it is challenging to disentangle their relative effects. Here, we surveyed the epibiota from 38 sympatric seaweed species that span diverse clades and have convergent morphology, which strongly influences seaweed ecology. Host identity explains most of the variation in epibiont communities and deeper host phylogenetic relationships (e.g., genus level) explain a small but significant portion of epibiont community variation. Strikingly, epibiota community composition is significantly influenced by host morphology and epibiota richness increases with morphological complexity of the seaweed host. This effect is robust after controlling for phylogenetic non-independence and is strongest for crustose seaweeds. We experimentally validated the effect of host morphology by quantifying bacterial community assembly on latex sheets cut to resemble three seaweed morphologies. The patterns match those observed in our field survey. Thus, biodiversity increases with habitat complexity in host-associated microbial communities, mirroring patterns observed in animal communities. We suggest that host morphology and structural complexity are underexplored mechanisms structuring microbial communities.Subject terms: Microbial ecology, Biodiversity     

A Global Phylogeny of Leafmining Ectoedemia Moths (Lepidoptera: Nepticulidae): Exploring Host Plant Family Shifts and Allopatry as Drivers of Speciation

Background

Host association patterns in Ectoedemia (Lepidoptera: Nepticulidae) are also encountered in other insect groups with intimate plant relationships, including a high degree of monophagy, a preference for ecologically dominant plant families (e.g. Fagaceae, Rosaceae, Salicaceae, and Betulaceae) and a tendency for related insect species to feed on related host plant species. The evolutionary processes underlying these patterns are only partly understood, we therefore assessed the role of allopatry and host plant family shifts in speciation within Ectoedemia.

Methodology

Six nuclear and mitochondrial DNA markers with a total aligned length of 3692 base pairs were used to infer phylogenetic relationships among 92 species belonging to the subgenus Ectoedemia of the genus Ectoedemia, representing a thorough taxon sampling with a global coverage. The results support monophyletic species groups that are congruent with published findings based on morphology. We used the obtained phylogeny to explore host plant family association and geographical distribution to investigate if host shifts and allopatry have been instrumental in the speciation of these leafmining insects.

Significance

We found that, even though most species within species groups commonly feed on plants from one family, shifts to a distantly related host family have occasionally occurred throughout the phylogeny and such shifts are most commonly observed towards Betulaceae. The largest radiations have occurred within species groups that feed on Fagaceae, Rosaceae, and Salicaceae. Most species are restricted to one of the seven global biogeographic regions, but within species groups representatives are commonly found in different biogeographic regions. Although we find general patterns with regard to host use and biogeography, there are differences between clades that suggest that different drivers of speciation, and perhaps drivers that we did not examine, have shaped diversity patterns in different clades.     

Phylogenetic analysis of trophic associations

Ecologists frequently collect data on the patterns of association between adjacent trophic levels in the form of binary or quantitative food webs. Here, we develop statistical methods to estimate the roles of consumer and resource phylogenies in explaining patterns of consumer-resource association. We use these methods to ask whether closely related consumer species are more likely to attack the same resource species and whether closely related resource species are more likely to be attacked by the same consumer species. We then show how to use estimates of phylogenetic signals to predict novel consumer-resource associations solely from the phylogenetic position of species for which no other (or only partial) data are available. Finally, we show how to combine phylogenetic information with information about species' ecological characteristics and life-history traits to estimate the effects of species traits on consumer-resource associations while accounting for phylogenies. We illustrate these techniques using a food web comprising species of parasitoids, leaf-mining moths, and their host plants.     

Polyphagy and diversification in tussock moths: Support for the oscillation hypothesis from extreme generalists

Theory on plasticity driving speciation, as applied to insect–plant interactions (the oscillation hypothesis), predicts more species in clades with higher diversity of host use, all else being equal. Previous support comes mainly from specialized herbivores such as butterflies, and plasticity theory suggests that there may be an upper host range limit where host diversity no longer promotes diversification. The tussock moths (Erebidae: Lymantriinae) are known for extreme levels of polyphagy. We demonstrate that this system is also very different from butterflies in terms of phylogenetic signal for polyphagy and for use of specific host orders. Yet we found support for the generality of the oscillation hypothesis, in that clades with higher diversity of host use were found to contain more species. These clades also consistently contained the most polyphagous single species. Comparing host use in Lymantriinae with related taxa shows that the taxon indeed stands out in terms of the frequency of polyphagous species. Comparative evidence suggests that this is most probably due to its nonfeeding adults, with polyphagy being part of a resulting life history syndrome. Our results indicate that even high levels of plasticity can drive diversification, at least when the levels oscillate over time.     

Pre‐Patch Experience Affects the Egg Distribution Pattern in a Polyembryonic Parasitoid of Moth Egg Batches

According to foraging theory, female parasitoids should alter their host choice in response to cues that indicate a limitation of resources. We tested whether females of the polyembryonic parasitoid Ageniaspis fuscicollis (Hymenoptera: Encyrtidae), which attack egg batches of small ermine moths (Lepidoptera: Yponomeutidae), would alter their host acceptance pattern in response to different pre‐patch experience. We kept females of the parasitoid prior to a patch visit under different conditions, which should indicate different levels of competition for hosts. With increased competition as pre‐patch experience, females laid more eggs per host egg and self‐superparasitized more often, and the resultant egg distributions showed a trend from more regular distributions to increasingly Poisson and aggregated distributions. Consequently, females with a pre‐patch experience that would indicate low competition for hosts had the most even egg distributions. We conclude that pre‐patch experience of competitors may lead to a significant change of mutual interference patterns in egg‐laying A. fuscicollis wasps.     

LARGE‐SCALE EVOLUTIONARY PATTERNS OF HOST PLANT ASSOCIATIONS IN THE LEPIDOPTERA

We characterized evolutionary patterns of host plant use across about 2500 species of British Lepidoptera, using character optimization and independent phylogenetic contrasts among 95 operational taxa, and evaluated the extent to which caterpillars are monophagous, use woody host plants, and feed concealed. We also analyzed the use of different Angiosperm superorders and related these associations to other key variables. The Nepticulidae, Pterophoridae, and Gracillariidae allowed explicit comparisons between the British fauna and the Lepidoptera worldwide, which indicated that our broad categorizations for Britain are accurate predictors for the global fauna. The first (lower glossatan) radiation of the Lepidoptera started with monophagous, internal feeding on woody Eurosids I. Polyphagy on nonwoody Eurosids I evolved together with the ability to feed externally, but did initially not produce significant radiations. Exposed feeding became associated with radiations in the lower Ditrysia and Apoditrysia and remained correlated with more polyphagy, fewer woody host plants, and increasing use of other Angiosperm superorders. The macrolepidopteran radiation has frequent reversals to monophagy on woody Eurosids I, particularly in taxa that lost concealed feeding. We discuss the general implications of these results and address several key adaptations and constraints that have characterized the major transitions in lepidopteran life histories.     

Allopatric distribution and diversification without niche shift in a bryophyte-feeding basal moth lineage (Lepidoptera: Micropterigidae)

The Lepidoptera represent one of the most successful radiations of plant-feeding insects, which predominantly took place within angiosperms beginning in the Cretaceous period. Angiosperm colonization is thought to underlie the evolutionary success of the Lepidoptera because angiosperms provide an enormous range of niches for ecological speciation to take place. By contrast, the basal lepidopteran lineage, Micropterigidae, remained unassociated with angiosperms since Jurassic times but nevertheless achieved a modest diversity in the Japanese Archipelago. We explored the causes and processes of diversification of the Japanese micropterigid moths by performing molecular phylogenetic analysis and extensive ecological surveying. Phylogenetic analysis recovered a monophyletic group of approximately 25 East Asian endemic species that feed exclusively on the liverwort Conocephalum conicum, suggesting that niche shifts hardly played a role in their diversification. Consistent with the low flying ability of micropterigid moths, the distributions of the Conocephalum specialists are each localized and allopatric, indicating that speciation by geographical isolation has been the major process shaping the diversity of Japanese Micropterigidae. To our knowledge, this is the largest radiation of herbivorous insects that does not accompany any apparent niche differentiation. We suggest that the significance of non-ecological speciation during the diversification of the Lepidoptera is commonly underestimated.     

Effect of learning on the oviposition preference of field-collected and laboratory-reared Chilo partellus (Lepidoptera: Crambidae) populations

Recent studies show that Vetiver grass, (Vetiveria zizanioides (L.) Nash), may have potential as a dead-end trap crop in an overall habitat management strategy for the spotted stem borer, Chilo partellus (Swinhoe) (Lepidoptera: Crambidae). Vetiver grass is highly preferred for oviposition, in spite of the fact that larval survival is extremely low on this grass. The oviposition behaviour of female Chilo partellus moths was investigated by determining the amount and size of egg batches allocated to maize and Vetiver plants and studying the effect of rearing conditions and oviposition experience on host plant selection. Two-choice preference tests were used to examine the effect of experience of maize (a suitable host plant) and Vetiver plants on the oviposition choice of C. partellus. For both field-collected and laboratory-reared moths, no significant differences were found in the preference distributions between the experienced groups. It is concluded that females do not learn, i.e. that they do not change their preference for Vetiver grass after having experienced oviposition on either maize or this grass, which supports the idea that trap cropping could have potential as a control method for C. partellus. Differences observed between field-collected and laboratory-reared moths in the amount and size of egg batches laid on maize and Vetiver grass indicate that data obtained from experiments with laboratory-reared insects should be treated with caution.