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Rubin B.E.R.,University of Chicago | Moreau C.S.,Integrative Research Center
Nature Communications | Year: 2016

Symbiosis-the close and often long-Term interaction of species-is predicted to drive genome evolution in a variety of ways. For example, parasitic interactions have been shown to increase rates of molecular evolution, a trend generally attributed to the Red Queen Hypothesis. However, it is much less clear how mutualisms impact the genome, as both increased and reduced rates of change have been predicted. Here we sequence the genomes of seven species of ants, three that have convergently evolved obligate plant-Ant mutualism and four closely related species of non-mutualists. Comparing these sequences, we investigate how genome evolution is shaped by mutualistic behaviour. We find that rates of molecular evolution are higher in the mutualists genome wide, a characteristic apparently not the result of demography. Our results suggest that the intimate relationships of obligate mutualists may lead to selective pressures similar to those seen in parasites, thereby increasing rates of evolution. © The Author(s) 2016.

Huang J.-P.,University of Michigan | Huang J.-P.,Integrative Research Center
Molecular Ecology | Year: 2016

The prevalence and consequences of genetic introgression between species have been intensively debated. I used Hercules beetles as examples to test for conditions that may be associated with the occurrence of introgression. RADseq data were used to reconstruct the species tree and history of introgression between Hercules beetles. Image data from museum specimens were used to investigate the phenotypic similarity of two adaptive traits between species from two distinct climatic realms (Nearctic vs. Neotropical). Genetic introgression was identified between Hercules beetles living in geographic proximity (parapatric). Phylogenetic relatedness and phenotypic similarity did not predict nor preclude genetic introgression between species. Phenotypic assimilation in body coloration was evident between distantly related Hercules beetles codistributed in Central America, where directional introgression was also statistically supported from the putative donor to receiver lineages. The number of introgressed loci was significantly higher between species with than without phenotypic similarity. I discuss the implications of recent studies on adaptive genetic introgression by providing supporting evidence from the Hercules beetle system. © 2016 John Wiley & Sons Ltd

Angielczyk K.D.,Integrative Research Center | Schmitz L.,Pitzer and Scripps Colleges
Proceedings of the Royal Society B: Biological Sciences | Year: 2014

Nocturnality is widespread among extant mammals and often considered the ancestral behavioural pattern for all mammals. However, mammals are nested within a larger clade, Synapsida, and non-mammalian synapsids comprise a rich phylogenetic, morphological and ecological diversity. Even though non-mammalian synapsids potentially could elucidate the early evolution of diel activity patterns and enrich the understanding of synapsid palaeobiology, data on their diel activity are currently unavailable. Using scleral ring and orbit dimensions, we demonstrate that nocturnal activity was not an innovation unique to mammals but a character that appeared much earlier in synapsid history, possibly several times independently. The 24 Carboniferous to Jurassic non-mammalian synapsid species in our sample featured eye morphologies consistent with all major diel activity patterns, with examples of nocturnality as old as the Late Carboniferous (ca 300 Ma). Carnivores such as Sphenacodon ferox and Dimetrodon milleri, but also the herbivorous cynodont Tritylodon longaevus were likely nocturnal, whereas most of the anomodont herbivores are reconstructed as diurnal. Recognizing the complexity of diel activity patterns in non-mammalian synapsids is an important step towards a more nuanced picture of the evolutionary history of behaviour in the synapsid clade. © 2014 The Author(s) Published by the Royal Society. All rights reserved.

Maestri R.,Federal University of Rio Grande do Sul | Patterson B.D.,Integrative Research Center
PLoS ONE | Year: 2016

Understanding the spatial distribution of species sheds light on the group's biogeographical history, offers clues to the drivers of diversity, and helps to guide conservation strategies. Here, we compile geographic range information for South America's diverse rodents, whose 14 families comprise ~50% of the continent's mammalian species. The South American rodent fauna is dominated by independent and temporally staggered radiations of caviomorph and sigmodontine groups.We mapped species richness and turnover of all rodents and the principal clades to identify the main predictors of diversity patterns. Species richness was highest in the Andes, with a secondary hotspot in Atlantic Forest and some regions of considerable richness in Amazonia. Differences in richness were evident between the caviomorphs and sigmodontines, the former showing the greatest richness in tropical forests whereas the latter show-and largely determine-the all-rodent pattern. Elevation was the main predictor of sigmodontine richness, whereas temperature was the principal variable correlated with richness of caviomorphs. Across clades, species turnover was highest along the Andes and was best explained by elevational relief. In South America, the effects of the familiar latitudinal gradient in species richness are mixed with a strong longitudinal effect, triggered by the importance of elevation and the position of the Andes. Both latitudinal and elevational effects help explain the complicated distribution of rodent diversity across the continent. The continent's restricted-range species-those seemingly most vulnerable to localized disturbance-are mostly distributed along the Andes and in Atlantic Forest, with the greatest concentration in Ecuador. Both the Andes and Atlantic Forest are known hotspots for other faunal and floral components. Contrasting patterns of the older caviomorph and younger sigmodontine radiations underscore the interplay of both historical and ecological factors in determining present-day diversity patterns. © 2016 Maestri, Patterson. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Cox C.B.,Forge Cottage | Angielczyk K.D.,Integrative Research Center
Journal of Vertebrate Paleontology | Year: 2015

Cranial material of the dicynodont Endothiodon from the middle fossiliferous horizon of the Permian Ruhuhu Formation (Ruhuhu Basin, Tanzania) is described as a new species, E. tolani. Endothiodon tolani is distinguished from other Endothiodon species by the absence of a pineal boss and the presence of tusks in most specimens. Although some parts of the Ruhuhu Formation probably correlate with the Eodicynodon or Tapinocephalus assemblage zones of the South African Karoo Basin, it is uncertain whether E. tolani is older than E. bathystoma or E. Mahalanobisi. There is less evidence for extensive anteroposterior translation of the mandible in E. tolani than in other dicynodonts. The jaw joint is specialized for allowing some medial-lateral motion. Mastication involved unilateral chewing. Flexure of the postdentary bones relative to the fused dentaries permitted the posterolaterally directed rows of teeth on one side of the skull and mandible to move past one another. The long tooth rows and prominent horn-covered ridges and grooves on the palate and mandible of Endothiodon are unique among dicynodonts. Comparisons with other taxa suggest that its feeding system may have been specialized for cutting three-dimensional objects such as stems or rhizomes. The dicynodont feeding system is very stereotyped throughout the clade's history, but Endothiodon escaped the constraints that affected other dicynodonts, allowing it to evolve a unique skull morphology. This evolutionary flexibility did not translate into high taxonomic richness (we recognize only three species of Endothiodon), but Endothiodon was able to achieve high levels of relative abundance in some basins.

Voight J.R.,Integrative Research Center
Journal of Molluscan Studies | Year: 2015

Bivalves of the families Teredinidae and Xylophagaidae bore into and eat wood in shallow water and the deep sea, respectively. After an introduction to these sister taxa, I consider how they bore, focussing on the evolution of the cephalic hood in teredinids, which could contribute to the depth separation between the families. If the hood serves as a counter pressure to the foot, it may be vital in allowing teredinids to bore wood that contains air. The availability of wood has been suggested to determine the distribution of these animals. Mangrove habitats with abundant wood sustain the highest diversity, about one-third of all known teredinids. The open ocean, where wood is all but nonexistent, presents a nearly impassable barrier to most wood borers. Only after wooden sailing ships transported teredinids between ports did introduced species become problematic. Despite the rarity of wood in the open ocean, some xylophagaids live there as, it is hypothesized, do a limited number of teredinids; wood in the open ocean is predicted to be large because large size enhances buoyancy. The life history of open-ocean species may differ fundamentally from that of nearshore species. Physical stressors of temperature, salinity and desiccation appear to affect teredinids minimally; xylophagaids on the seafloor do not experience these variables. How biotic interactions such as competition and predation affect wood borers is yet to be thoroughly studied, but their impact may be greater than has been recognized, especially among teredinids. Although humans regard teredinids as pests that destroy wooden structures, and attempt to eradicate them from some areas, these animals play vital ecological roles. Teredinids make the energy and nutrients locked into wood available to the local community. Xylophagaids are nearly unique in breaking down cellulose and are analogous to primary producers in sustaining the diverse deep-sea wood-fall communities. The survival of borers requires wood to be present. The reduction of trees near water courses, removal of driftwood from navigable rivers and the destruction and fragmentation of the world's mangrove habitats all threaten the predictable supply of wood in the sea and may seriously threaten the survival of these molluscs. © 2015 © The Author 2015. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved.

Roopnarine P.D.,California Academy of Sciences | Angielczyk K.D.,Integrative Research Center
Science | Year: 2015

The fossil record contains exemplars of extreme biodiversity crises. Here, we examined the stability of terrestrial paleocommunities from South Africa during Earth's most severe mass extinction, the Permian-Triassic.We show that stability depended critically on functional diversity and patterns of guild interaction, regardless of species richness. Paleocommunities exhibited less transient instability-relative to model communities with alternative community organization-and significantly greater probabilities of being locally stable during the mass extinction. Functional patterns that have evolved during an ecosystem's history support significantly more stable communities than hypothetical alternatives.

Hunt G.,Smithsonian Institution | Hopkins M.J.,American Museum of Natural History | Lidgard S.,Integrative Research Center
Proceedings of the National Academy of Sciences of the United States of America | Year: 2015

Previous analyses of evolutionary patterns, or modes, in fossil lineages have focused overwhelmingly on three simple models: stasis, random walks, and directional evolution. Here we use likelihood methods to fit an expanded set of evolutionary models to a large compilation of ancestor-descendant series of populations from the fossil record. In addition to the standard three models, we assess more complex models with punctuations and shifts from one evolutionary mode to another. As in previous studies, we find that stasis is common in the fossil record, as is a strict version of stasis that entails no real evolutionary changes. Incidence of directional evolution is relatively low (13%), but higher than in previous studies because our analytical approach can more sensitively detect noisy trends. Complex evolutionary models are often favored, overwhelmingly so for sequences comprising many samples. This finding is consistent with evolutionary dynamics that are, in reality, more complex than any of the models we consider. Furthermore, the timing of shifts in evolutionary dynamics varies among traits measured from the same series. Finally, we use our empirical collection of evolutionary sequences and a long and highly resolved proxy for global climate to inform simulations in which traits adaptively track temperature changes over time. When realistically calibrated, we find that this simple model can reproduce important aspects of our paleontological results. We conclude that observed paleontological patterns, including the prevalence of stasis, need not be inconsistent with adaptive evolution, even in the face of unstable physical environments. © 2015, National Academy of Sciences. All rights reserved.

Voight J.R.,Integrative Research Center
American Malacological Bulletin | Year: 2014

Hydrothermal vents in the deep sea are harsh, temporally unpredictable habitats with what appears to be a distinct fauna. Decades of subsea research with crewed and remote vehicles have generated a list of known species; is the species list complete? Evidence derived from mollusks sampled at hydrothermal vents on the East Pacific Rise (EPR), and Gorda and Juan de Fuca ridges suggests that the answer is yes. A 2006 compilation of hydrothermal vent species based on decades of research is updated and compared to specimens from these three active ridges in collections of the Field Museum of Natural History (FMNH) that resulted from limited collecting activity. Only three dives at each of the two Gorda Ridge vents collected all named species; 90% of the 20 species known from Juan de Fuca Ridge were collected in nine cruises. At the EPR, only 81% of the 43 known species were collected, but differences among the ridges were not significant. The limited FMNH collections increased the known ranges of six species from Juan de Fuca to Gorda Ridge and of nine species on the EPR. In addition, the EPR appears to host more rare species, potentially due to the frequent temporal changes at these vents. Mollusks currently known from each ridge, with their expanded ranges, are listed; the implications of these results for recent discoveries of slow-spreading vent fields are discussed. © 2014, BioOne. All rights reserved.

Cai C.-Y.,CAS Nanjing Institute of Geology and Palaeontology | Thayer M.K.,Integrative Research Center | Engel M.S.,University of Kansas | Newton A.F.,Integrative Research Center | And 4 more authors.
Proceedings of the National Academy of Sciences of the United States of America | Year: 2014

The reconstruction and timing of the early stages of social evolution, such as parental care, in the fossil record is a challenge, as these behaviors often do not leave concrete traces. One of the intensely investigated examples of modern parental care are the modern burying beetles (Silphidae: Nicrophorus), a lineage that includes notable endangered species. Here we report diverse transitional silphids from the Mesozoic of China and Myanmar that provide insights into the origins of parental care. Jurassic silphids from Daohugou, sharing many defining characters of Nicrophorinae, primitively lack stridulatory files significant for parental care communications; although morphologically similar, Early Cretaceous nicrophorines from the Jehol biota possess such files, indicating that a system of parental care had evolved by this early date. More importantly, burying beetles of the genus Nicrophorus have their earliest first record in mid-Cretaceous Burmese amber, and document early evolution of elaborate biparental care and defense of small vertebrate carcasses for their larvae. Parental care in the Early Cretaceous may have originated from competition between silphids and their predators. The rise of the Cretaceous Nicrophorinae implies a biology similar to modern counterparts that typically feed on carcasses of small birds and mammals.

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