THE EVOLUTION OF AGRICULTURE IN BEETLES (CURCULIONIDAE: SCOLYTINAE AND PLATYPODINAE)

Abstract Beetles in the weevil subfamilies Scolytinae and Platypodinae are unusual in that they burrow as adults inside trees for feeding and oviposition. Some of these beetles are known as ambrosia beetles for their obligate mutualisms with asexual fungi—known as ambrosia fungi—that are derived from plant pathogens in the ascomycete group known as the ophiostomatoid fungi. Other beetles in these subfamilies are known as bark beetles and are associated with free‐living, pathogenic ophiostomatoid fungi that facilitate beetle attack of phloem of trees with resin defenses. Using DNA sequences from six genes, including both copies of the nuclear gene encoding enolase, we performed a molecular phylogenetic study of bark and ambrosia beetles across these two subfamilies to establish the rate and direction of changes in life histories and their consequences for diversification. The ambrosia beetle habits have evolved repeatedly and are unreversed. The subfamily Platypodinae is derived from within the Scolytinae, near the tribe Scolytini. Comparison of the molecular branch lengths of ambrosia beetles and ambrosia fungi reveals a strong correlation, which a fungal molecular clock suggests spans 60 to 21 million years. Bark beetles have shifted from ancestral association with conifers to angiosperms and back again several times. Each shift to angiosperms is associated with elevated diversity, whereas the reverse shifts to conifers are associated with lowered diversity. The unusual habit of adult burrowing likely facilitated the diversification of these beetle‐fungus associations, enabling them to use the biomass‐rich resource that trees represent and set the stage for at least one origin of eusociality.     

The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles

Transitions from fresh to saline habitats are restricted to a handful of insect lineages, as the colonization of saline waters requires specialized mechanisms to deal with osmotic stress. Previous studies have suggested that tolerance to salinity and desiccation could be mechanistically and evolutionarily linked, but the temporal sequence of these adaptations is not well established for individual lineages. We combined molecular, physiological and ecological data to explore the evolution of desiccation resistance, hyporegulation ability (i.e., the ability to osmoregulate in hyperosmotic media) and habitat transitions in the water beetle genus Enochrus subgenus Lumetus (Hydrophilidae). We tested whether enhanced desiccation resistance evolved before increases in hyporegulation ability or vice versa, or whether the two mechanisms evolved in parallel. The most recent ancestor of Lumetus was inferred to have high desiccation resistance and moderate hyporegulation ability. There were repeated shifts between habitats with differing levels of salinity in the radiation of the group, those to the most saline habitats generally occurring more rapidly than those to less saline ones. Significant and accelerated changes in hyporegulation ability evolved in parallel with smaller and more progressive increases in desiccation resistance across the phylogeny, associated with the colonization of meso‐ and hypersaline waters during global aridification events. All species with high hyporegulation ability were also desiccation‐resistant, but not vice versa. Overall, results are consistent with the hypothesis that desiccation resistance mechanisms evolved first and provided the physiological basis for the development of hyporegulation ability, allowing these insects to colonize and diversify across meso‐ and hypersaline habitats.     

Diversity, distinctiveness and conservation status of the Mediterranean coastal dung beetle assemblage in the Regional Natural Park of the Camargue (France)

The Mediterranean region as a whole has the highest dung beetle species richness within Europe. Natural coastal habitats in this region are among those which have suffered severe human disturbance. We studied dung beetle diversity and distinctiveness within one of the most important coastal protected areas in the west Euro‐Mediterranean region (the regional Park of Camargue, southern France) and made comparisons of dung beetle assemblages with other nearby Mediterranean localities, as well as with other coastal protected area (Doñana National Park, Spain). Our finding showed that: (1) The species richness of coastal habitats in the Camargue is low and only grasslands showed a similar level of species richness and abundance to inland habitats of other Mediterranean localities. The unique habitats of the coastal area (beaches, dunes and marshes) are largely colonized by species widely distributed in the hinterland. (2) In spite of their low general distinctiveness, dune and marsh edges are characterized by the occurrence of two rare, vulnerable, specialized and large roller dung beetle species of the genus Scarabaeus. As with other Mediterranean localities, current findings suggest a recent decline of Scarabaeus populations and the general loss of coastal dung beetle communities in Camargue. (3) The comparison of dung beetle assemblages between the Camargue and Doñana shows that, in spite of the low local dung beetle species richness in the Camargue, the regional dung beetle diversity is similar between both protected areas. Unique historical and geographical factors can explain the convergence in regional diversity as well as the striking divergence in the composition of dung beetle assemblages between both territories.     

Factors influencing the geographical distribution of Dendroctonus rhizophagus (Coleoptera: Curculionidae: Scolytinae) in the Sierra Madre Occidental, México

The bark beetle, Dendroctonus rhizophagus Thomas & Bright, is endemic to the Sierra Madre Occidental (SMOC) in México. This bark beetle is a major pest of the seedlings and young saplings of several pine species that are of prime importance to the nation's forest industry. Despite the significance of this bark beetle as a pest, its biology, ecology, and distribution are poorly known. Three predictive modeling approaches were used as a first approximation to identify bioclimatic variables related to the presence of D. rhizophagus in the SMOC and to obtain maps of its potential distribution within the SMOC, which is a morphotectonic province. Our results suggest that the bark beetle could have an almost continuous distribution throughout the major mountain ranges of the SMOC. This beetle has a relatively narrow ecological niche with respect to some temperature and precipitation variables and inhabits areas with climatic conditions that are unique from those usually prevalent in the SMOC. However, the bark beetle has a broad ecological niche with respect to the number of hosts that it attacks. At the macro-scale level, the D. rhizophagus distribution occurs within the wider distribution of its main hosts. The limit of the geographical distribution of this bark beetle coincides with the maximum temperature isotherms. Our results imply a preference for temperate habitats, which leads to the hypothesis that even minor changes in climate may have significant effects on its distribution and abundance.     

Hystrignathus dearmasi sp. n. (Oxyurida, Hystrignathidae), first record of a nematode parasitizing a Panamanian Passalidae (Insecta, Coleoptera)

Hystrignathus dearmasi sp. n. (Oxyurida: Hystrignathidae) is described from an unidentified passalid beetle (Coleoptera: Passalidae) from Panama. It resembles Hystrignathus cobbi Travassos & Kloss, 1957 from Brazil, by having a similar form of the cephalic end, extension of cervical spines and absence of lateral alae. It differs from the latter species by having the body shorter, the oesophagus and tail comparatively larger, the vulva situated more posterior and the eggs ridged. This species constitutes the first record of a nematode parasitizing a Panamanian passalid.     

Repeated evolution of amphibious behavior in fish and its implications for the colonization of novel environments

We know little about on how frequently transitions into new habitats occur, especially the colonization of novel environments that are the most likely to instigate adaptive evolution. One of the most extreme ecological transitions has been the shift in habitat associated with the move from water to land by amphibious fish. We provide the first phylogenetic investigation of these transitions for living fish. Thirty‐three families have species reported to be amphibious and these are likely independent evolutionary origins of fish emerging onto land. Phylogenetic reconstructions of closely related taxa within one of these families, the Blenniidae, inferred as many as seven convergences on a highly amphibious lifestyle. Taken together, there appear to be few constraints on fish emerging onto land given amphibious behavior has evolved repeatedly many times across ecologically diverse families. The colonization of novel habitats by other taxa resulting in less dramatic changes in environment should be equally, if not, more frequent in nature, providing an important prerequisite for subsequent adaptive differentiation.     

Endosymbiosis

The phenomenon of endosymbiosis, or one organism living within another, has deeply impacted the evolution of life and continues to shape the ecology of countless species. Traditionally, biologists have viewed evolution as a largely bifurcating pattern, reflecting mutations and other changes in existing genetic information and the occasional speciation and divergence of lineages. While lineage bifurcation has clearly been important in evolution, the merging of two lineages through endosymbiosis has also made profound contributions to evolutionary novelty. Mitochondria and chloroplasts are relicts of ancient bacterial endosymbionts that ultimately extended the range of acceptable habitats for life by allowing hosts to thrive in the presence of oxygen and to convert light into energy. Today, the sheer abundance of endosymbiotic relationships across diverse host lineages and habitats testifies to their continued significance.     

Habitat structure and the evolution of diffusible siderophores in bacteria

Bacteria typically rely on secreted metabolites, potentially shareable at the community level, to scavenge resources from the environment. The evolution of diffusible, shareable metabolites is, however, difficult to explain because molecules can get lost, or be exploited by cheating mutants. A key question is whether natural selection can act on molecule structure to control loss and shareability. We tested this possibility by collating information on diffusivity properties of 189 secreted iron‐scavenging siderophores and the natural habitats occupied by the siderophore‐producing species. In line with evolutionary theory, we found that highly diffusible siderophores have preferentially evolved in species living in structured habitats, such as soil and hosts, because structuring can keep producers and their shareable goods together. Poorly diffusible siderophores, meanwhile, have preferentially evolved in species living in unstructured habitats, such as seawater, indicating that these metabolites are less shareable and more likely provide direct benefits to the producers.     

Does the composition of Scarabaeidae (Coleoptera) communities reflect the extent of land use changes in the Brazilian Amazon?

Scarab beetles (Coleoptera: Scarabaeidae) have been used to investigate the effects of environmental disturbances on forest structure and diversity. This group is recognized as sensitive to habitat perturbations and ecosystem changes. Here we examine the effects of anthropogenic impacts on Scarabaeidae composition, testing the following hypotheses: (1) Scarab beetle communities react to land use disturbances with predictable trends, (2) disturbed habitats are able to retain only a part of the Scarab beetle community of native forests or late secondary forests; (3) habitats largely differ in terms of species richness, taxonomic diversity and ecological composition, supporting exclusive and indicator species. We selected areas of native forest, agriculture, pasture for extensive livestock and secondary forests in different stages of regeneration. Our results show that the Scarabaeidae species were not indifferent to the gradient of structural changes represented by the studied areas. In fact, their patterns of habitat preference reveals communities more abundant and diverse in pristine habitats. In contrast, disturbed habitats, dominated by agricultural activities and pasture, indicated clear detrimental effects on the abundance of all forest Scarab beetle specialists. On the other hand, the generalist species, mainly associated with open environments, seemed to be favoured by the prevailing conditions induced by agricultural activities. Overall, the composition of the Scarab beetle communities is variable and sensitive to those structural gradients and, therefore, capable of responding as useful ecological indicators for assessing the extent of land use change or degradation.     

On the functions of stridulation by the passalid beetle Odontotaenius disjunctus (Coleoptera: Passalidae)

Crows (Corvus brachyrhynchos) are more hesitant to continue attacking and take longer to kill and eat stridulating passalid beetles (Odontotaenius disjunctus) than silenced beetles. This is an experimental demonstration of the deterrent capability of disturbance stridulation by an insect that has no active defences against the predator. Stridulation is not necessary for congregation by colony members. Silenced beetles congregate as effectively as controls. There is no evidence that the disturbance stridulation causes predictable responses in other colony members of this presocial beetle.     

A comparison of Passalidae (Coleoptera, Lamellicornia) diversity and community structure between primary and secondary tropical forest in Los Tuxtlas, Veracruz, Mexico

Comparison of the diversity and community structure of Coleoptera (Passalidae) collected in Los Tuxtlas, Veracruz, Mexico, in primary and secondary tropical forest has been carried out. The saproxylophagous beetles studied can be differentiated according to their presence in three distinct microhabitats of rotting logs: underbark, sapwood—heartwood and microhabitat generalists. Over the 2-year study period, 12 passalid species were recorded (six Passalini and six Proculini) represented by a total of 2971 individuals, collected from 234 rotting logs. The rarefaction method, the lognormal species—abundance relationship, and the nonparametric jackknife method were used to compare species richness between the habitats. The data were also fitted to log series, truncated lognormal, geometric, and broken-stick species abundance models to detect changes in community structure. The community composition of Passalidae in Los Tuxtlas did not differ ostensibly between the primary and secondary forests. Neither the mean number of individuals nor the biomass per log differed significantly. Furthermore, there were no significant differences between the two habitats in terms of the number of underbark, sapwood/heartwood, and microhabitat generalist species. Different richness estimators indicated that the primary forest community is only slightly richer. The slight decrease in richness of the secondary forest is related to a decrease in dominance by certain species, as well as to a more balanced abundance distribution, which is adequately described by the broken-stick model. Complementary explanations for this pattern may be: (1) that logging reduces the abundance of dominant species, thus preventing competitive exclusion in the secondary forest; and (2) that passalid diversity is not regulated by the diversity of tree species.     

Enemies in low places - insects avoid winter mortality and egg parasitism by modulating oviposition height

Oviposition site selection in insects is essential in terms of low egg mortality, high offspring survival and therefore a high reproductive output. Although oviposition height could be a crucial factor for the fitness of overwintering eggs, it has rarely been investigated. In this study the oviposition height of a polyphagous leaf beetle, Galeruca tanaceti Linnaeus in different habitats and at different times of the season was examined and its effect on egg clutch mortality was recorded. The leaf beetle occurs as an occasional pest on several agricultural plants. It deposits its eggs within herbaceous vegetation in autumn. Eggs are exposed to numerous biotic and abiotic mortality factors summarized as egg parasitism and winter mortality. Oviposition height of the leaf beetle was not uniform, but changed significantly with the structure of the habitat and during the season. Mean oviposition height per site (70.2+/-4.9 cm) was significantly higher than mean vegetation height (28.4+/-2.4 cm). Height of plants with egg clutches attached and oviposition height were significantly positively correlated. The results suggest that females try to oviposit as high as possible in the vegetation and on the plants selected. In accordance with this, the probability of egg parasitism and of winter egg clutch mortality significantly declined with increasing oviposition height. A preference of G. tanaceti for oviposition sites high up in the vegetation might therefore have evolved due to selection pressures by parasitoids and winter mortality.     

Flight Distance and Eye Size in Birds

Larger eyes capture more information from the environment than small eyes, but also require more brain space for information processing. Therefore, individuals have to optimize the size of their eyes, leading to the prediction that larger eyes should have evolved in species with greater benefits from large eyes, such as species subject to intense predation risk. In a comparative analysis of 97 bird species, we found that species that fled at longer distances from an approaching potential predator indeed had relatively large eyes for their body size. In contrast, there was no indication that large eyes had evolved in species living in secluded habitats, or in species eating mobile prey. These findings are consistent with the assumption that eye size is labile and can evolve in response to changing predator environments. They also suggest that eye size may act as a constraint on optimal anti‐predator behavior, if the predator community changes as a consequence of introductions or invasions.     

The relationship between the classification of Scottish ground beetle assemblages (Coleoptera, Carabidae) and the National Vegetation Classification of British plant communities

A sufficiently large body of knowledge on British ground beetle (Carabidae) communities now exists to allow investigation of whether habitats may be classified or described on the basis of their ground beetle communities, in the same way that the National Vegetation Classification (NVC) describes British plant communities. A data set of ground beetle abundances from pitfall traps at 481 sites in a range of natural, semi-natural and agricultural habitats throughout Scotland was available for analysis. Multivariate analysis (detrended correspondence analysis and fuzzy cluster analysis) was carried out on proportional catch data of 156 species of ground beetle from 444 of these sites and the results related to the NVC of the sites.
Initial analysis classified the sites into five broad categories: 1) peatlands, 2) calcifugous, 3) mesotrophic, 4) dry river sediments and 5) damp river sediments. Further analysis identified 15 ground beetle assemblages, each corresponding to a relatively well defined vegetation type within one of these broad categories. The major environmental factors appearing to determine the distribution of ground beetle assemblages were substratum type, disturbance and soil moisture, all of which are also important determinants of the distribution of plant communities. The presence and absence of relatively stenotopic species were important discriminants of certain habitats such as wetlands and river sediments but the relative abundances within assemblages of more eurytopic species provided good indications of a relationship between ground beetle assemblages and NVC categories.     

Microorganisms in the gut of beetles: evidence from molecular cloning

We have regularly cultured yeasts from the gut of certain beetles in our ongoing research. In this study cloned PCR products amplified from the gut contents of certain mushroom-feeding and wood-ingesting beetles in four families (Erotylidae, Tenebrionidae, Ciidae, and Passalidae) were sequenced and compared with culture results. Cultural techniques detected some yeasts present in the gut of the beetles, including a Pichia stipitis-like yeast associated with wood-ingesting passalid beetles. Clone sequences similar to several ascomycete yeasts and Malassezia restricta, a fastidious basidiomycetous yeast requiring special growth media, however, were not detected by culturing. Unexpectedly, phylogenetic analysis of additional clone sequences discovered from passalid beetles showed similarity to members of the Parabasalia, protists known from other wood-ingesting insects, termites, and wood roaches. Examination of all gut regions of living passalids, however, failed to reveal parabasalids, and it is possible that they were parasites in the gut tissue present in low numbers.     

Elongated hindguts in desert‐living dung beetles (Scarabaeidae: Scarabaeinae) feeding on dry dung pellets or plant litter

Most adult dung beetles (Scarabaeidae: Scarabaeinae) feed on fresh, wet dung of larger herbivorous or omnivorous mammals. As refractory plant fragments are selected out before ingestion, the food is presumed easily digestible. However, members of the desert‐living scarabaeine genus Pachysoma (probably evolved from an ancestor closely related to the wet‐dung feeding genus Scarabaeus) select dry dung pellets and/or plant litter. Thus, they ingest a much higher proportion of structural plant material, which nevertheless appears to be digested rather efficiently. This study investigates morphological modifications of the gut for this digestion in adults of eight Pachysoma species, both pellet and litter feeders. To ascertain hypothesized ancestral conditions, four fresh‐dung feeding Scarabaeus species were also examined. The latter have the usual dung beetle gut consisting of a long, simple midgut, followed by an equally simple, much shorter hindgut of the same width. Lengths of midguts (M) and hindguts (H) divided by body length (B) for comparison between species of different size are: 4.9–6.3 (M/B) and 0.7–0.8 (H/B), which is normal for dung feeders. In Pachysoma, lengths are 6.3–6.5 (M/B) and 1.0–1.4 (H/B) in pellet feeders, and 4.4–5.0 (M/B) and 2.0–2.5 (H/B) for litter feeders. Hindguts are still morphologically undifferentiated and of midgut width, but clearly longer, particularly in litter feeders. Presumably, plant fragments in the food are digested, at least partly, in the hindgut. If so, the morphological adaptation is unusual: simple elongation rather than the expansion of part of the hindgut, as found in several other plant‐ or detritus‐feeding scarabaeids. J. Morphol. 2013. © 2013 Wiley Periodicals, Inc.