Faster-haplodiploid evolution under divergence-with-gene-flow: Simulations and empirical data from pine-feeding hymenopterans.

Although haplodiploidy is widespread in nature, the evolutionary consequences of this mode of reproduction are not well characterized. Here, we examine how genome-wide hemizygosity and a lack of recombination in haploid males affects genomic differentiation in populations that diverge via natural selection while experiencing gene flow. First, we simulated diploid and haplodiploid "genomes" (500-kb loci) evolving under an isolation-with-migration model with mutation, drift, selection, migration and recombination; and examined differentiation at neutral sites both tightly and loosely linked to a divergently selected site. As long as there is divergent selection and migration, sex-limited hemizygosity and recombination cause elevated differentiation (i.e., produce a "faster-haplodiploid effect") in haplodiploid populations relative to otherwise equivalent diploid populations, for both recessive and codominant mutations. Second, we used genome-wide single nucleotide polymorphism data to model divergence history and describe patterns of genomic differentiation between sympatric populations of Neodiprion lecontei and N. pinetum, a pair of pine sawfly species (order: Hymenoptera; family: Diprionidae) that are specialized on different pine hosts. These analyses support a history of continuous gene exchange throughout divergence and reveal a pattern of heterogeneous genomic differentiation that is consistent with divergent selection on many unlinked loci. Third, using simulations of haplodiploid and diploid populations evolving according to the estimated divergence history of N. lecontei and N. pinetum, we found that divergent selection would lead to higher differentiation in haplodiploids. Based on these results, we hypothesize that haplodiploids undergo divergence-with-gene-flow and sympatric speciation more readily than diploids.

Development, implementation and impact of a new preprint solicitation process at Proceedings B.

Preprints are manuscripts posted on a public server that do not yet have formal certification of peer review from a scholarly journal. The increasingly prominent online repositories for these preprints provide a means of rapidly making scientific results accessible to all with an Internet connection. We here describe the catalysis and subsequent development of a successful new process to solicit preprints for consideration for publication in Proceedings B. We present preliminary comparisons between the focal topics and geographic origin of submitting authors of papers submitted in the traditional (non-solicited) route versus solicited preprints. This analysis suggests that the solicitation process seems to be achieving one of the primary goals of the preprint solicitation endeavour: broadening the scope of the papers featured in Proceedings B. We also use an informal survey of the early-career scientists that are or have been involved with the Preprint Editorial Team to find that these scientists view their participation positively with respect to career development and knowledge in their field. The inclusion of early-career researchers from across the world in the preprint solicitation process could also translate into social justice benefits by providing a career-building opportunity and a window into the publishing process for young scientists.

Host shifting and host sharing in a genus of specialist flies diversifying alongside their sunflower hosts.

Congeneric parasites are unlikely to specialize on the same tissues of the same host species, likely because of strong multifarious selection against niche overlap. Exceptions where >1 congeneric species use the same tissues reveal important insights into ecological factors underlying the origins and maintenance of diversity. Larvae of sunflower maggot flies in the genus Strauzia feed on plants in the family Asteraceae. Although Strauzia tend to be host specialists, some species specialize on the same hosts. To resolve the origins of host sharing among these specialist flies, we used reduced representation genomic sequencing to infer the first multilocus phylogeny of genus Strauzia. Our results show that Helianthus tuberosus and Helianthus grosseserratus each host three different Strauzia species and that the flies co-occurring on a host are not one another's closest relatives. Though this pattern implies that host sharing is most likely the result of host shifts, these may not all be host shifts in the conventional sense of an insect moving onto an entirely new plant. Many hosts of Strauzia belong to a clade of perennial sunflowers that arose 1-2 MYA and are noted for frequent introgression and hybrid speciation events. Our divergence time estimates for all of the Helianthus-associated Strauzia are within this same time window (<1 MYA), suggesting that rapid and recent adaptive introgression and speciation in Helianthus may have instigated the diversification of Strauzia, with some flies converging upon a single plant host after their respective ancestral host plants hybridized to form a new sunflower species.

Long-distance dispersal, ice sheet dynamics and mountaintop isolation underlie the genetic structure of glacier ice worms.

Disentangling the contemporary and historical factors underlying the spatial distributions of species is a central goal of biogeography. For species with broad distributions but little capacity to actively disperse, disconnected geographical distributions highlight the potential influence of passive, long-distance dispersal (LDD) on their evolutionary histories. However, dispersal alone cannot completely account for the biogeography of any species, and other factors-e.g. habitat suitability, life history-must also be considered. North American ice worms ( Mesenchytraeus solifugus) are ice-obligate annelids that inhabit coastal glaciers from Oregon to Alaska. Previous studies identified a complex biogeographic history for ice worms, with evidence for genetic isolation, unexpectedly close relationships among geographically disjunct lineages, and contemporary migration across large (e.g. greater than 1500 km) areas of unsuitable habitat. In this study, we analysed genome-scale sequence data for individuals from most of the known ice worm range. We found clear support for divergence between populations along the Pacific Coast and the inland flanks of the Coast Mountains (mean FST = 0.60), likely precipitated by episodic ice sheet expansion and contraction during the Pleistocene. We also found support for LDD of ice worms from Alaska to Vancouver Island, perhaps mediated by migrating birds. Our results highlight the power of genomic data for disentangling complex biogeographic patterns, including the presence of LDD.

Quantifying the unquantifiable: why Hymenoptera, not Coleoptera, is the most speciose animal order.

BACKGROUND: We challenge the oft-repeated claim that the beetles (Coleoptera) are the most species-rich order of animals. Instead, we assert that another order of insects, the Hymenoptera, is more speciose, due in large part to the massively diverse but relatively poorly known parasitoid wasps. The idea that the beetles have more species than other orders is primarily based on their respective collection histories and the relative availability of taxonomic resources, which both disfavor parasitoid wasps. Though it is unreasonable to directly compare numbers of described species in each order, the ecology of parasitic wasps-specifically, their intimate interactions with their hosts-allows for estimation of relative richness. RESULTS: We present a simple logical model that shows how the specialization of many parasitic wasps on their hosts suggests few scenarios in which there would be more beetle species than parasitic wasp species. We couple this model with an accounting of what we call the "genus-specific parasitoid-host ratio" from four well-studied genera of insect hosts, a metric by which to generate extremely conservative estimates of the average number of parasitic wasp species attacking a given beetle or other insect host species. CONCLUSIONS: Synthesis of our model with data from real host systems suggests that the Hymenoptera may have 2.5-3.2× more species than the Coleoptera. While there are more described species of beetles than all other animals, the Hymenoptera are almost certainly the larger order.

History, geography and host use shape genomewide patterns of genetic variation in the redheaded pine sawfly (Neodiprion lecontei).

Divergent host use has long been suspected to drive population differentiation and speciation in plant-feeding insects. Evaluating the contribution of divergent host use to genetic differentiation can be difficult, however, as dispersal limitation and population structure may also influence patterns of genetic variation. In this study, we use double-digest restriction-associated DNA (ddRAD) sequencing to test the hypothesis that divergent host use contributes to genetic differentiation among populations of the redheaded pine sawfly (Neodiprion lecontei), a widespread pest that uses multiple Pinus hosts throughout its range in eastern North America. Because this species has a broad range and specializes on host plants known to have migrated extensively during the Pleistocene, we first assess overall genetic structure using model-based and model-free clustering methods and identify three geographically distinct genetic clusters. Next, using a composite-likelihood approach based on the site frequency spectrum and a novel strategy for maximizing the utility of linked RAD markers, we infer the population topology and date divergence to the Pleistocene. Based on existing knowledge of Pinus refugia, estimated demographic parameters and patterns of diversity among sawfly populations, we propose a Pleistocene divergence scenario for N. lecontei. Finally, using Mantel and partial Mantel tests, we identify a significant relationship between genetic distance and geography in all clusters, and between genetic distance and host use in two of three clusters. Overall, our results indicate that Pleistocene isolation, dispersal limitation and ecological divergence all contribute to genomewide differentiation in this species and support the hypothesis that host use is a common driver of population divergence in host-specialized insects.

Multiple mechanisms contribute to isolation by environment in the redheaded pine sawfly, Neodiprion lecontei.

Isolation by environment (IBE) is a population genomic pattern that arises when ecological barriers reduce gene flow between populations. Although current evidence suggests IBE is common in nature, few studies have evaluated the underlying mechanisms that generate IBE patterns. In this study, we evaluate five proposed mechanisms of IBE (natural selection against immigrants, sexual selection against immigrants, selection against hybrids, biased dispersal, and environment-based phenological differences) that may give rise to host-associated differentiation within a sympatric population of the redheaded pine sawfly, Neodiprion lecontei, a species for which IBE has previously been detected. We first characterize the three pine species used by N. lecontei at the site, finding morphological and chemical differences among the hosts that could generate divergent selection on sawfly host-use traits. Next, using morphometrics and ddRAD sequencing, we detect modest phenotypic and genetic differentiation among sawflies originating from different pines that is consistent with recent, in situ divergence. Finally, via a series of laboratory assays-including assessments of larval performance on different hosts, adult mate and host preferences, hybrid fitness, and adult eclosion timing-we find evidence that multiple mechanisms contribute to IBE in N. lecontei. Overall, our results suggest IBE can emerge quickly, possibly due to multiple mechanisms acting in concert to reduce migration between different environments.

The impact of life stage and pigment source on the evolution of novel warning signal traits.

Our understanding of how novel warning color traits evolve in natural populations is largely based on studies of reproductive stages and organisms with endogenously produced pigmentation. In these systems, genetic drift is often required for novel alleles to overcome strong purifying selection stemming from frequency-dependent predation and positive assortative mating. Here, we integrate data from field surveys, predation experiments, population genomics, and phenotypic correlations to explain the origin and maintenance of geographic variation in a diet-based larval pigmentation trait in the redheaded pine sawfly (Neodiprion lecontei), a pine-feeding hymenopteran. Although our experiments confirm that N. lecontei larvae are indeed aposematic-and therefore likely to experience frequency-dependent predation-our genomic data do not support a historical demographic scenario that would have facilitated the spread of an initially deleterious allele via drift. Additionally, significantly elevated differentiation at a known color locus suggests that geographic variation in larval color is currently maintained by selection. Together, these data suggest that the novel white morph likely spread via selection. However, white body color does not enhance aposematic displays, nor is it correlated with enhanced chemical defense or immune function. Instead, the derived white-bodied morph is disproportionately abundant on a pine species with a reduced carotenoid content relative to other pine hosts, suggesting that bottom-up selection via host plants may have driven divergence among populations. Overall, our results suggest that life stage and pigment source can have a substantial impact on the evolution of novel warning signals, highlighting the need to investigate diverse aposematic taxa to develop a comprehensive understanding of color variation in nature.

Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both.

Quantifying the frequency of shifts to new host plants within diverse clades of specialist herbivorous insects is critically important to understand whether and how host shifts contribute to the origin of species. Oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise a tribe of ∼1000 species of phytophagous insects that induce gall formation on various organs of trees in the family Fagacae-primarily the oaks (genus Quercus; ∼435 sp.). The association of oak gall wasps with oaks is ancient (∼50 my), and most oak species are galled by one or more gall wasp species. Despite the diversity of both gall wasp species and their plant associations, previous phylogenetic work has not identified the strong signal of host plant shifting among oak gall wasps that has been found in other phytophagous insect systems. However, most emphasis has been on the Western Palearctic and not the Nearctic where both oaks and oak gall wasps are considerably more species rich. We collected 86 species of Nearctic oak gall wasps from most of the major clades of Nearctic oaks and sequenced >1000 Ultraconserved Elements (UCEs) and flanking sequences to infer wasp phylogenies. We assessed the relationships of Nearctic gall wasps to one another and, by leveraging previously published UCE data, to the Palearctic fauna. We then used phylogenies to infer historical patterns of shifts among host tree species and tree organs. Our results indicate that oak gall wasps have moved between the Palearctic and Nearctic at least four times, that some Palearctic wasp clades have their proximate origin in the Nearctic, and that gall wasps have shifted within and between oak tree sections, subsections, and organs considerably more often than previous data have suggested. Given that host shifts have been demonstrated to drive reproductive isolation between host-associated populations in other phytophagous insects, our analyses of Nearctic gall wasps suggest that host shifts are key drivers of speciation in this clade, especially in hotspots of oak diversity. Although formal assessment of this hypothesis requires further study, two putatively oligophagous gall wasp species in our dataset show signals of host-associated genetic differentiation unconfounded by geographic distance, suggestive of barriers to gene flow associated with the use of alternative host plants.