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Although the genetic consequences of contemporary landscape composition and range shifts driven Pleistocene climatic oscillations have been studied fairly well in alpine organisms, we know much less about how these factors have shaped the demography of taxa with broader climatic niches and distributions. Here, we use high-throughput sequencing data to study the processes underlying spatial patterns of genomic variation in Omocestus panteli (Bolívar, 1887) (Orthoptera: Acrididae), a common Iberian grasshopper distributed across numerous habitat types and a wide elevational range (from sea level to >2,000 m). Although the species is broadly distributed, our analyses support that its contemporary populations show significant genetic fragmentation that dates back to the last glacial period. Accordingly, spatially explicit testing of alternative gene flow scenarios and demographic inference analyses revealed that genetic differentiation between populations and their long-term effective population sizes are best explained by the spatial configuration of environmentally suitable habitats during the last glacial maximum (ca. 21 ka). At that time, the species experienced net demographic expansions but interspersed unsuitable areas might have disrupted gene flow and created opportunity for geographical diversification. Collectively, our analyses indicate that the genetic makeup of contemporary populations is not well explained by current environmental factors or geographical barriers to dispersal but mostly reflects genetic fragmentation during the last glacial period followed by postglacial admixture among previously isolated gene pools. Taken together, these results support that the Pleistocene ‘species pump’ model might be also useful in explaining demographic dynamics and geographical diversification in taxa characterized by broad climatic niches.
Biogeographic clines in morphology along environmental gradients can illuminate forces influencing trait evolution within and between species. Latitude has long been studied as a driver of morphological clines, with a focus on body size and temperature. However, counteracting environmental pressures may impose constraints on body size. In montane landscapes, declines in air density with elevation can negatively impact flight performance in volant species, which may contribute to selection for reduced body mass despite declining temperatures. We examine morphology in two bumble bee (Hymenoptera: Apidae: Bombus Latreille) species, Bombus vancouverensis Cresson and Bombus vosnesenskii Radoszkowski, across mountainous regions of California, Oregon, and Washington, United States. We incorporate population genomic data to investigate the relationship between genomic ancestry and morphological divergence. We find that B. vancouverensis, which tends to be more specialized for high elevations, exhibits stronger spatial-environmental variation, being smaller in the southern and higher elevation parts of its range and having reduced wing loading (mass relative to wing area) at high elevations. Bombus vosnesenskii, which is more of an elevational generalist, has substantial trait variation, but spatial-environmental correlations are weak. Population structure is stronger in the smaller B. vancouverensis, and we find a significant association between elevation and wing loading after accounting for genetic structure, suggesting the possibility of local adaptation for this flight performance trait. Our findings suggest that some conflicting results for body size trends may stem from distinct environmental pressures that impact different aspects of bumble bee ecology, and that different species show different morphological clines in the same region.
MOLECULAR PHYLOGENETICS, PHYLOGENOMICS, AND PHYLOGEOGRAPHY
Large-scale global efforts on DNA barcoding have repeatedly revealed unexpected patterns of variability in mtDNA, including deep intraspecific divergences and haplotype sharing between species. Understanding the evolutionary causes behind these patterns calls for insights from the nuclear genome. While building a near-complete DNA barcode library of Finnish caddisflies, a case of barcode-sharing and some cases of deep intraspecific divergences were observed. In this study, the Apatania zonella (Zetterstedt, 1840) group and three Limnephilus Leach, 1815 species were studied using double digest RAD sequencing (ddRAD-seq), morphology, and DNA barcoding.The results support the present species boundaries in the A. zonella group species. A morphologically distinct but mitogenetically nondistinct taxon related to parthenogenetic Apatania hispida (Forsslund, 1930) got only weak support for its validity as a distinct species. The morphology and genomic-scale data do not indicate cryptic diversity in any of the three Limnephilus species despite the observed deep intraspecific divergences in DNA barcodes. This demonstrates that polymorphism in mtDNA may not reflect cryptic diversity, but mitonuclear discordance due to other evolutionary causes.
In the 21st century, phylogeography has experienced dramatic growth in the data and methods used by the field. Insect (more generally, hexapod) phylogeography has contributed to major advances and many of the influential papers included hexapods as model systems. In this literature review, we: (i) highlight recent phylogeographic work in hexapod systems, and (ii) identify broader trends and critical future steps in the field. We include a summary of useful methodological approaches and identify the methods used to approach different questions asked in phylogeographic studies. An updated summary of the applications that phylogeography has contributed to the field of entomology, including spatial studies, conservation, systematics, pest control, and invasive species, is included to highlight vital work in the field. Special attention is devoted to investigations which seek to use multi-species data to understand community ecological and evolutionary processes. Finally, we overview the main challenges, opportunities, and emerging areas, highlighting the “phylogeographic shortfall” that exists between the number of described hexapod species vs. the number of species that have been the focus of phylogeographic investigation.
La filogeografía del siglo XXI demuestra un crecimiento fuerte y sostenido en la integración y expansión de fronteras en relación al uso de datos y desarrollos metodológicos. La filogeografía de insectos (y en forma más general, de hexápodos) ha contribuido a avances mayores de la disciplina, con varios trabajos filogeográficos fundamentales tratando modelos de hexápodos. Esta revisión de la literatura tiene dos objetivos: i) realzar y tratar estudios filogeográficos recientes en insectos y hexápodos y ii) evaluar sus resultados principales para así identificar tendencias generales y oportunidades futuras. Con el fin de asistir en la selección de métodos apropiados a aquellos interesados en estos estudios, comenzamos haciendo una revisión de los métodos filogeográficos existentes, presentando también una guía para asistir en su selección. Después de esta revisión metodológica, presentamos un resumen general de aplicaciones recientes en entomología, demostrando, entre otros, su importancia en áreas tales como estudios geoespaciales, conservación, sistemática, control de plagas y de especies invasoras. Siguiendo en esta línea, revisamos las contribuciones únicas de la filogeografía entomológica en estudios comparados, conectando ecología de comunidades con procesos evolutivos, siendo esta una de las áreas más activas y prometedoras de la filogeografía actual. Finalmente, discutimos los mayores desafíos, oportunidades y áreas emergentes de la filogeografía contemporánea, e identificamos el “déficit filogeográfico” existente entre la cantidad de especies de hexápodos descritas y aquellas que han recibido atención en estudios filogeográficos.
Animal body size has important evolutionary implications. The wolf spider genus Schizocosa Chamberlin, 1904 has developed as a model for studies on courtship, with visual and vibratory signals receiving attention; however, body size has never been carefully evaluated. Although species of Schizocosa can be distinguished from their close relatives by differences in genitalic structures, male ornamentation, and behavior, some species are morphologically similar, making diagnosis, and identification difficult. Evaluation of species boundaries using genetic data across Schizocosa is limited. The similar species S. maximaDondale & Redner, 1978 and S. mccooki (Montgomery, 1904) are separated predominantly on the basis of size differences, with S. maxima being larger. We evaluate the evolution of size in these two Schizocosa species distributed in western North America, where gigantism of S. maxima is hypothesized to occur, particularly in California. We sampled subgenomic data (RADseq) and inferred the phylogeny of S. mccooki, S. maxima, and relatives. We apply a variational autoencoder machine learning approach to visualize population structuring within widespread S. mccooki and evaluate size within the context of a comparative phylogenetic framework to test the hypotheses related to genetic clustering of populations and gigantism. Our data show S. mccooki populations are not genealogically exclusive with respect to S. maxima. Likewise, S. maxima individuals are not recovered as a lineage and do not form an isolated genetic cluster, suggesting that the observed differences in size cannot be used to accurately delimit species. The cause of gigantism in S. maxima remains unexplained, but provides a framework for future studies of size variation and speciation.
Alena Sucháčková Bartoňová, Martin Konvička, Jana Marešová, Dana Bláhová, David Číp, Pavel Skala, Miloš Andres, Vladimír Hula, Matthias Dolek, Adi Geyer, Oliver Böck, Tomáš Kadlec, Zdeněk Faltýnek Fric
Central European dry grasslands represent extrazonal patches of the Eurasian steppe biome. They suffer from severe habitat alterations due to land-use changes, abandonment, or inappropriate management.The butterflies Chazara briseis (Linnaeus, 1764) (Lepidoptera: Nymphalidae), Polyommatus damon (Denis & Schiffermüller, 1775) (Lepidoptera: Lycaenidae), and Polyommatus dorylas (Denis & Schiffermüller, 1775) (Lepidoptera: Lycaenidae), specialized inhabitants of these steppe patches, are all swiftly disappearing from Central Europe. We reviewed data on the recent history of their population retractions in the region, including conservation efforts. Using samples from their whole distribution ranges, we sequenced and analyzed COI and wingless genes and together with Species Distribution Modelling reconstructed their biogeographic histories. Populations of C. briseis expanded over the Eurasian steppe biome, where large ungulates maintained extensive grasslands with short open sward. Polyommatus damon became widespread in the steppes during glacial times, and retracted during interglacials, resembling cold-adapted species. It is limited by too dry weather, and it requires disturbed grassland followed by temporal abandonment. Its present genetic structure was induced by the major Pleistocene Mountain glaciations. Polyommatus dorylas prefers an oceanic climate and populated Central Europe from the Balkans during the Holocene. The species depends on disturbed ground. Currently, all three species inhabit only a few remnant sites in Central Europe, and their populations have been further declining in recent years.Targeted conservation actions, including habitat management at remaining sites, ex situ breeding, and (re)introductions, are being taken in Austria, the Czech Republic, and Germany.
Comparative phylogeographic studies can distinguish between idiosyncratic and community-wide responses to past environmental change. However, to date, the impacts of species interactions have been largely overlooked. Here we used non-genetic data to characterize two competing scenarios about expected levels of congruence among five deadwood-associated (saproxylic) invertebrate species (i.e., a wood-feeding cockroach, termite, and beetle; a predatory centipede, and a detritivorous millipede) from the southern Appalachian Mountains—a globally recognized center of endemism. Under one scenario, abiotic factors primarily drove species' responses, with predicted congruence based on the spatial overlap of climatically stable habitat areas estimated for each species via ecological niche modeling.The second scenario considered biotic factors to be most influential, with proxies for species interactions used to predict congruence. Analyses of mitochondrial and nuclear DNA sequences focused on four axes of comparison: the number and geographic distribution of distinct spatial-genetic clusters, phylogeographic structure, changes in effective population size, and historical gene flow dynamics. Overall, we found stronger support for the ecological co-associations scenario, suggesting an important influence of biotic factors in constraining or facilitating species' responses to Pleistocene climatic cycles. However, there was an imperfect fit between predictions and outcomes of genetic data analyses.Thus, while thought-provoking, conclusions remain tentative until additional data on species interactions becomes available. Ultimately, the approaches presented here advance comparative phylogeography by expanding the scope of inferences beyond solely considering abiotic drivers, which we believe is too simplistic. This work also provides conservation-relevant insights into the evolutionary history of a functionally important ecological community.
The cold-tolerant leaf beetle Gonioctena quinquepunctata displays a large but fragmented European distribution and is restricted to mountain regions in the southern part of its range. Using a RAD-seq-generated large single nucleotide polymorphism (SNP) data set (> 10,000 loci), we investigated the geographic distribution of genetic variation within the Vosges mountains (eastern France), where the species is common.To translate this pattern of variation into an estimate of its capacity to disperse, we simulated SNP data under a spatially explicit model of population evolution (essentially a grid overlapping a map, in which each cell is considered a different population) and compared the simulated and real data with an approximate Bayesian computation (ABC) approach. For this purpose, we assessed a new SNP statistic, the DSVSF (distribution of spatial variation in SNP frequencies) that summarizes genetic variation in a spatially explicit context, and compared its usefulness to standard statistics often used in population genetic analyses. A test of our overall strategy was conducted with simulated data and showed that it can provide a good estimate of the level of dispersal of an organism over its geographic range. The results of our analyses suggested that this insect disperses well within the Vosges mountains, much more than was initially expected given the current and probably past fragmentation of its habitat and given the results of previous studies on genetic variation in other mountain leaf beetles.
Visual systems in animals often conspicuously reflect the demands of their ecological interactions. Ants occupy a wide range of terrestrial microhabitats and ecological roles. Additionally, ant eye morphology is highly variable; species range from eyeless subterranean-dwellers to highly visual predators or desert navigators. Through a comparative approach spanning 64 species, we evaluated the relationship between ecology and eye morphology on a wide taxonomic scale. Using worker caste specimens, we developed two- and three-dimensional measurements to quantify eye morphology and position, as well as antennal scape length. Surprisingly, we find limited associations between ecology and most eye traits, however, we recover significant relationships between antennal scape length and some vision-linked attributes. While accounting for shared ancestry, we find that two- and three-dimensional eye area is correlated with foraging niche and ommatidia density is significantly associated with trophic level in our sample of ant taxa. Perhaps signifying a resource investment tradeoff between visual and olfactory or tactile acuity, we find that ommatidia density is negatively correlated with antennal scape length. Additionally, we find that eye position is significantly related to antennal scape length and also report a positive correlation between scape length and eye height, which may be related to the shared developmental origin of these structures. Along with previously known relationships between two-dimensional eye size and ant ecology, our results join reports from other organismal lineages suggesting that morphological traits with intuitive links to ecology may also be shaped by developmental restrictions and energetic trade-offs.
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