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Data from: Life-stage differences in spatial genetic structure in an irruptive forest insect: implications for dispersal and spatial synchrony
James, Patrick M. A.; Cooke, Barry; Brunet, Bryan; Lumley, Lisa; Sperling, Felix; Fortin, Marie-Josée; Quinn, Vanessa S.; Sturtevant, Brian R.; Brunet, Bryan M. T.; Lumley, Lisa M.; Sperling, Felix A. H. — 2014-12-03 Dispersal determines the flux of individuals, energy, and information and is therefore a key determinant of ecological and evolutionary dynamics. Yet, it remains difficult to quantify its importance relative to other factors. This is particularly true in cyclic populations in which demography, drift, and dispersal contribute to spatio-temporal variability in genetic structure. Improved understanding of how dispersal influences spatial genetic structure is needed to disentangle the multiple processes that give rise to spatial synchrony in irruptive species. In this study, we examined spatial genetic structure in an economically important irruptive forest insect, the spruce budworm (Choristoneura fumiferana) to better characterize how dispersal, demography, and ecological context interact to influence spatial synchrony in a localized outbreak. We characterized spatial variation in microsatellite allele frequencies using 231 individuals and 7 geographic locations. We show that: (1) gene flow among populations is likely very high (Fst ≈ 0); (2) despite an overall low level of genetic structure, important differences exist between adult (moth) and juvenile (larvae) life-stages; and (3) the localized outbreak is the likely source of moths captured elsewhere in our study area. This study demonstrates the potential of using molecular methods to distinguish residents from migrants and for understanding how dispersal contributes to spatial synchronization. In irruptive populations, the strength of genetic structure depends on the timing of data collection (e.g., trough vs. peak), location, and dispersal. Taking into account this ecological context allows us to make more general characterizations of how dispersal can affect spatial synchrony in irruptive populations.
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Data from: Distinct sources of gene flow produce contrasting population genetic dynamics at different range boundaries of a Choristoneura budworm
Blackburn, Gwylim S.; Brunet, Bryan M. T.; Muirhead, Kevin; Cusson, Michel; Béliveau, Catherine; Levesque, Roger C.; Lumley, Lisa M.; Sperling, Felix A. H. — 2017-10-27 Populations are often exposed to multiple sources of gene flow, but accounts are lacking of the population genetic dynamics that result from these interactions or their effects on local evolution. Using a genomic clines framework applied to 1195 SNPs, we documented genome-wide, locus-specific patterns of introgression between Choristoneura occidentalis biennis spruce budworms and two ecologically divergent relatives, C. o. occidentalis and C. fumiferana, that it interacts with at alternate boundaries of its range. We observe contrasting hybrid indexes between these hybrid zones, no overlap in ‘gene flow outliers’ (clines showing relatively extreme extents or rates of locus-specific introgression), and variable linkage disequilibrium among those outliers. At the same time, correlated genome-wide rates of introgression between zones suggest the presence of processes common to both boundaries. These findings highlight the contrasting population genetic dynamics that can occur at separate frontiers of a single population, while also suggesting that shared patterns may frequently accompany cases of divergence-with-gene-flow that involve a lineage in common. Our results point to potentially complex evolutionary outcomes for populations experiencing multiple sources of gene flow.
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Data from: Comparative phylogeography, genetic differentiation, and contrasting reproductive modes in three fungal symbionts of a multipartite bark beetle symbiosis
Roe, Amanda D.; Rice, Adrianne V.; Coltman, David W.; Cooke, Janice E. K.; Sperling, Felix A. H. — 2010-11-08 Multipartite symbioses are complex symbiotic relationships involving multiple interacting partners. These types of partnerships provide excellent opportunities in which to apply a comparative approach to identify common historical patterns of population differentiation and species-specific life history traits. Using three symbiotic blue stain fungal species (Ophiostomatacea) associated with outbreaking populations of the mountain pine beetle (Dendroctonus ponderosae Hopkins) in western Canada, we applied phylogenetic, population genetic, and demographic approaches to clarify phylogeographic patterns among the three fungal species. Broadly, the three species showed significant population differentiation, forming northern and southern populations, despite dramatic differences in haplotype diversity. Finer scale structuring and population demographic patterns were less consistent, showing some interspecific incongruence. By contrasting these species simultaneously, we were able to identify differences in recombination rate and ecological traits that can explain the observed patterns of incongruence among the fungal species. By applying a comparative approach to partners of a multipartite symbiosis we were able to distinguish congruent population structuring and species-specific differences that help us to understand the complexity and evolution of this symbiotic system.
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Data from: Molecular phylogeny of the diverse parasitoid wasp genus Ophion Fabricius (Hymenoptera: Ichneumonidae: Ophioninae)
Schwarzfeld, Marla D.; Broad, Gavin R.; Sperling, Felix A. H. — 2016-04-27 Ophion Fabricius is a diverse genus of nocturnal ichneumonid wasps (Insecta: Hymenoptera) that is particularly species-rich in temperate areas, yet has received little taxonomic attention in the Holarctic region, where most species occur. While there have been some attempts to divide Ophion into monophyletic species groups, the vast majority of species have been lumped into a single, paraphyletic group, the O. luteus species group, which is defined only by the lack of characters specific to the other groups. The challenging morphology of this large catch-all group has limited attempts to subdivide it, and no phylogenetic hypothesis has been proposed for the genus as a whole. In this study, we use DNA sequence data [28S ribosomal RNA (28S), cytochrome oxidase 1 (COI) and internal transcribed spacer 2 (ITS2)] to present the first molecular phylogeny of Ophion. We also describe the secondary structure of ITS2 for the first time in Ichneumonidae, and explore its implications for phylogeny estimation. We define 13 species groups, nine of which were previously considered part of the O. luteus species group s.l. The included species groups are the O. minutus, O. areolaris, O. scutellaris, O. flavidus, O. parvulus, O. slossonae, O. nigrovarius, O. pteridis, O. luteus s.s., and O. obscuratus species groups, along with three groups lacking described species (Species group 1, New Zealand group, Madagascar group). This study provides a framework for future studies of this diverse and morphologically challenging genus.
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Data from: Adaptive and neutral markers both show continent-wide population structure of mountain pine beetle (Dendroctonus ponderosae)
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Batista, Philip D.; Janes, Jasmine K.; Boone, Celia K.; Murray, Brent W.; Sperling, Felix A. H. — 2017-08-04 Assessments of population genetic structure and demographic history have traditionally been based on neutral markers while explicitly excluding adaptive markers. In this study, we compared the utility of putatively adaptive and neutral single-nucleotide polymorphisms (SNPs) for inferring mountain pine beetle population structure across its geographic range. Both adaptive and neutral SNPs, and their combination, allowed range-wide structure to be distinguished and delimited a population that has recently undergone range expansion across northern British Columbia and Alberta. Using an equal number of both adaptive and neutral SNPs revealed that adaptive SNPs resulted in a stronger correlation between sampled populations and inferred clustering. Our results suggest that adaptive SNPs should not be excluded prior to analysis from neutral SNPs as a combination of both marker sets resulted in better resolution of genetic differentiation between populations than either marker set alone. These results demonstrate the utility of adaptive loci for resolving population genetic structure in a nonmodel organism.
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Data from: Comparison of five methods for delimitating species in Ophion Fabricius, a diverse genus of parasitoid wasps (Hymenoptera, Ichneumonidae)
Schwarzfeld, Marla D.; Sperling, Felix A. H.; Sperling, Felix A.H. — 2015-08-11 DNA taxonomy has been proposed as a method to quickly assess diversity and species limits in highly diverse, understudied taxa. Here we use five methods for species delimitation and two genetic markers (COI and ITS2) to assess species diversity within the parasitoid genus, Ophion. We searched for compensatory base changes (CBC’s) in ITS2, and determined that they are too rare to be of practical use in delimiting species in this genus. The other four methods used both COI and ITS2, and included distance-based (threshold analysis and ABGD) and tree-based (GMYC and PTP) models. We compared the results of these analyses to each other under various parameters and tested their performance with respect to 11 Nearctic species/morphospecies and 15 described Palearctic species. We also computed barcode accumulation curves of COI sequences to assess the completeness of sampling. The species count was highly variable depending on the method and parameters used, ranging from 47 to 168 species, with more conservative estimates of 89–121 species. Despite this range, many of the Nearctic test species were fairly robust with respect to method. We concluded that while there was often good congruence between methods, GMYC and PTP were less reliant on arbitrary parameters than the other two methods and more easily applied to genetic markers other than COI. However, PTP was less successful at delimiting test species than was GMYC. All methods, as well as the barcode accumulation curves, indicate that several Palearctic species remain undescribed and that we have scarcely begun to appreciate the Nearctic diversity within this genus.
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Data from: Cross-platform compatibility of de novo-aligned SNPs in a non-model butterfly genus
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Campbell, Erin O.; Davis, Corey S.; Dupuis, Julian R.; Muirhead, Kevin; Sperling, Felix A.H.; Sperling, Felix A. H. — 2017-06-20 High-throughput sequencing methods for genotyping genome-wide markers are being rapidly adopted for phylogenetics of non-model organisms in conservation and biodiversity studies. However, the reproducibility of SNP genotyping and degree of marker overlap or compatibility between datasets from different methodologies have not been tested in non-model systems. Using double-digest restriction site associated DNA sequencing, we sequenced a common set of 22 specimens from the butterfly genus Speyeria on two different Illumina platforms, using two variations of library preparation. We then used a de novo approach to bioinformatic locus assembly and SNP discovery for subsequent phylogenetic analyses. We found a high rate of locus recovery despite differences in library preparation and sequencing platforms, as well as overall high levels of data compatibility after data processing and filtering. These results provide the first application of NGS methods for phylogenetic reconstruction in Speyeria, and support the use and long-term viability of SNP genotyping applications in non-model systems.
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Data from: Population structure and migration pattern of a conifer pathogen, Grosmannia clavigera, as influenced by its symbiont the mountain pine beetle
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Tsui, Clement Kin Ming; Roe, Amanda D.; El-Kassaby, Yousry A.; Rice, Adrianne V.; Massoumi Alamouti, Sepideh; Sperling, Felix A. H.; Cooke, Janice E. K.; Bohlmann, Jörg; Hamelin, Richard C. — 2011-09-13 We investigated the population structure of Grosmannia clavigera (Gc), a fungal symbiont of the mountain pine beetle (MPB) that plays a crucial role in the establishment and reproductive success of this pathogen. This insect–fungal complex has destroyed over 16 million ha of lodgepole pine forests in Canada, the largest MPB epidemic in recorded history. During this current epidemic, MPB has expanded its range beyond historically recorded boundaries, both northward and eastward, and has now reached the jack pine of Alberta, potentially threatening the Canadian boreal forest. To better understand the dynamics between the beetle and its fungal symbiont, we sampled 19 populations in western North America and genotyped individuals from these populations with eight microsatellite markers. The fungus displayed high haplotype diversity, with over 250 unique haplotypes observed in 335 single spore isolates. Linkage equilibria in 13 of the 19 populations suggested that the fungus reproduces sexually. Bayesian clustering and distance analyses identified four genetic clusters that corresponded to four major geographical regions, which suggested that the epidemic arose from multiple geographical sources. A genetic cluster north of the Rocky Mountains, where the MPB has recently become established, experienced a population bottleneck, probably as a result of the recent range expansion. The two genetic clusters located north and west of the Rocky Mountains contained many fungal isolates admixed from all populations, possibly due to the massive movement of MPB during the epidemic. The general agreement in north–south differentiation of MPB and G. clavigera populations points to the fungal pathogen’s dependence on the movement of its insect vector. In addition, the patterns of diversity and the individual assignment tests of the fungal associate suggest that migration across the Rocky Mountains occurred via a northeastern corridor, in accordance with meteorological patterns and observation of MPB movement data. Our results highlight the potential of this pathogen for both expansion and sexual reproduction, and also identify some possible barriers to gene flow. Understanding the ecological and evolutionary dynamics of this fungus–beetle association is important for the modelling and prediction of MPB epidemics.
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Data from: Testing the role of the Red Queen and Court Jester as drivers of the macroevolution of Apollo butterflies
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Condamine, Fabien L.; Rolland, Jonathan; Höhna, Sebastian; Sperling, Felix A. H.; Sanmartín, Isabel — 2018-02-15 In macroevolution, the Red Queen (RQ) model posits that biodiversity dynamics depend mainly on species-intrinsic biotic factors such as interactions among species or life-history traits, while the Court Jester (CJ) model states that extrinsic environmental abiotic factors have a stronger role. Until recently, a lack of relevant methodological approaches has prevented the unraveling of contributions from these two types of factors to the evolutionary history of a lineage. Here we take advantage of the rapid development of new macroevolution models that tie diversification rates to changes in paleoenvironmental (extrinsic) and/or biotic (intrinsic) factors. We inferred a robust and fully-sampled species-level phylogeny, as well as divergence times and ancestral geographic ranges, and related these to the radiation of Apollo butterflies (Parnassiinae) using both extant (molecular) and extinct (fossil/morphological) evidence. We tested whether their diversification dynamics are better explained by a RQ or CJ hypothesis, by assessing whether speciation and extinction were mediated by diversity-dependence (niche filling) and clade-dependent host-plant association (RQ) or by large-scale continuous changes in extrinsic factors such as climate or geology (CJ). For the RQ hypothesis, we found significant differences in speciation rates associated with different host-plants but detected no sign of diversity-dependence. For CJ, the role of Himalayan-Tibetan building was substantial for biogeography but not a driver of high speciation, while positive dependence between warm climate and speciation/extinction was supported by continuously varying maximum-likelihood models. We find that rather than a single factor, the joint effect of multiple factors (biogeography, species traits, environmental drivers, and mass extinction) is responsible for current diversity patterns, and that the same factor might act differently across clades, emphasizing the notion of opportunity. This study confirms the importance of the confluence of several factors rather than single explanations in modeling diversification within lineages.
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Data from: Would an RRS by any other name sound as RAD?
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Campbell, Erin O.; Brunet, Bryan M.T.; Dupuis, Julian R.; Sperling, Felix A.H.; Brunet, Bryan M. T.; Sperling, Felix A. H. — 2019-06-11 1. Sampling markers throughout a genome with restriction enzymes emerged in the 2000s as reduced representation shotgun sequencing (RRS). Rapid advances in sequencing technology have since spurred modifications of RRS, giving rise to many derivatives with unique names, such as restriction site-associated DNA sequencing (RADseq). But naming conventions have often been more creative than consistent and criteria for recognizing unique methods have been unclear, resulting in a proliferation of names characterized by ambiguity. 2. We give an overview of methodological and etymological relationships among 36 restriction enzyme-based methods, and survey the consistency of references to five prominent methods in the literature. 3. We identified several instances of methodological convergence, and note that many published derivatives have modified only minor elements of parent protocols. Misattribution through ambiguous or inconsistent literature references was observed in 8.4% of journal articles citing the original one and two-enzyme RADseq and GBS, as well as SBG publications. 4. The rapid expansion of names associated with derivative protocols is confusing and, in many cases, unwarranted. We urge greater restraint in naming derivative methods and suggest general guidelines for naming that promote a balance between clarity, descriptiveness, and recognition of scientific innovation.

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(Author: Sperling, Felix A. H.)

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