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      Breaking out of biogeographical modules: range expansion and taxon cycles in the hyperdiverse ant genus Pheidole

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          Abstract

          Aim

          We sought to reconstruct the biogeographical structure and dynamics of a hyperdiverse ant genus, Pheidole, and to test several predictions of the taxon cycle hypothesis. Using large datasets on Pheidole geographical distributions and phylogeny, we (1) inferred patterns of biogeographical modularity (clusters of areas with similar faunal composition), (2) tested whether species in open habitats are more likely to be expanding their range beyond module boundaries, and (3) tested whether there is a bias of lineage flow from high‐ to low‐diversity areas.

          Location

          The Old World.

          Methods

          We compiled and jointly analysed a comprehensive database of Pheidole geographical distributions, the ecological affinities of different species, and a multilocus phylogeny of the Old World radiation. We used network modularity methods to infer biogeographical structure in the genus and comparative methods to evaluate the hypotheses.

          Results

          The network analysis identified eight biogeographical modules, and a suite of species with anomalous ranges that are statistically more likely to occur in open habitat, supporting the hypothesis that open habitats promote range expansion. Phylogenetic analysis shows evidence for a cascade pattern of colonization from Asia to New Guinea to the Pacific, but no ‘upstream’ colonization in the reverse direction.

          Main conclusions

          The distributions of Pheidole lineages in the Old World are highly modular, with modules generally corresponding to biogeographical regions inferred in other groups of organisms. However, some lineages have expanded their ranges across module boundaries, and these species are more likely to be adapted to open habitats rather than interior forest. In addition, there is a cascade pattern of dispersal from higher to lower diversity areas during these range expansions. Our findings are consistent with the taxon cycle hypothesis, although they do not rule out alternative interpretations.

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          Most cited references 9

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          Functional cartography of complex metabolic networks

           ,   (2005)
          High-throughput techniques are leading to an explosive growth in the size of biological databases and creating the opportunity to revolutionize our understanding of life and disease. Interpretation of these data remains, however, a major scientific challenge. Here, we propose a methodology that enables us to extract and display information contained in complex networks. Specifically, we demonstrate that one can (i) find functional modules in complex networks, and (ii) classify nodes into universal roles according to their pattern of intra- and inter-module connections. The method thus yields a ``cartographic representation'' of complex networks. Metabolic networks are among the most challenging biological networks and, arguably, the ones with more potential for immediate applicability. We use our method to analyze the metabolic networks of twelve organisms from three different super-kingdoms. We find that, typically, 80% of the nodes are only connected to other nodes within their respective modules, and that nodes with different roles are affected by different evolutionary constraints and pressures. Remarkably, we find that low-degree metabolites that connect different modules are more conserved than hubs whose links are mostly within a single module.
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            Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades.

            Founder-event speciation, where a rare jump dispersal event founds a new genetically isolated lineage, has long been considered crucial by many historical biogeographers, but its importance is disputed within the vicariance school. Probabilistic modeling of geographic range evolution creates the potential to test different biogeographical models against data using standard statistical model choice procedures, as long as multiple models are available. I re-implement the Dispersal-Extinction-Cladogenesis (DEC) model of LAGRANGE in the R package BioGeoBEARS, and modify it to create a new model, DEC + J, which adds founder-event speciation, the importance of which is governed by a new free parameter, [Formula: see text]. The identifiability of DEC and DEC + J is tested on data sets simulated under a wide range of macroevolutionary models where geography evolves jointly with lineage birth/death events. The results confirm that DEC and DEC + J are identifiable even though these models ignore the fact that molecular phylogenies are missing many cladogenesis and extinction events. The simulations also indicate that DEC will have substantially increased errors in ancestral range estimation and parameter inference when the true model includes + J. DEC and DEC + J are compared on 13 empirical data sets drawn from studies of island clades. Likelihood-ratio tests indicate that all clades reject DEC, and AICc model weights show large to overwhelming support for DEC + J, for the first time verifying the importance of founder-event speciation in island clades via statistical model choice. Under DEC + J, ancestral nodes are usually estimated to have ranges occupying only one island, rather than the widespread ancestors often favored by DEC. These results indicate that the assumptions of historical biogeography models can have large impacts on inference and require testing and comparison with statistical methods. © The Author(s) 2014. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: journals.permissions@oup.com.
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              Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads.

              Recent studies have identified range expansion as a potential driver of speciation. Yet it remains poorly understood how, under identical extrinsic settings, differential tendencies for geographic movement of taxa originate and subsequently affect diversification. We identified multiple traits that predict large distributional ranges in extant species of toads (Bufonidae) and used statistical methods to define and phylogenetically reconstruct an optimal range-expansion phenotype. Our results indicate that lineage-specific range-shifting abilities increased through an accumulation of adaptive traits that culminated in such a phenotype. This initiated the episode of global colonization and triggered the major radiation of toads. Evolution toward a range-expansion phenotype might be crucial to understanding both ancient widespread radiations and the evolutionary background of contemporary invasive species such as the cane toad.
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                Author and article information

                Journal
                J Biogeogr
                J. Biogeogr
                10.1111/(ISSN)1365-2699
                JBI
                Journal of Biogeography
                John Wiley and Sons Inc. (Hoboken )
                0305-0270
                1365-2699
                01 September 2015
                December 2015
                : 42
                : 12 ( doiID: 10.1111/jbi.2015.42.issue-12 )
                : 2289-2301
                Affiliations
                [ 1 ]Okinawa Institute of Science and Technology Graduate University 1919‐1 Tancha Onna‐son Okinawa 904‐0495Japan
                [ 2 ] Department of Ecology & Evolutionary BiologyMuseum of Zoology University of Michigan Ann Arbor MIUSA
                [ 3 ] Department of EntomologyUniversity of Illinois at Urbana‐Champaign Chicago ILUSA
                [ 4 ] Biology CentreCzech Academy of Sciences České BudějoviceCzech Republic
                [ 5 ] Department of BiologyUniversity of Guanajuato GuanajuatoMexico
                [ 6 ] Department of Bioinformatics and GenomicsUniversity of North Carolina at Charlotte Charlotte NCUSA
                [ 7 ] Department of ZoologyTyumen State University TyumenRussia
                [ 8 ] Committee on Evolutionary BiologyUniversity of Chicago Chicago ILUSA
                [ 9 ]CSIRO Land & Water Flagship Darwin NTAustralia
                [ 10 ] Department of Entomology & NematologyUniversity of Florida Gainesville FLUSA
                [ 11 ] Department of BiologyUniversity of Rochester Rochester NYUSA
                [ 12 ] Museum of Comparative ZoologyHarvard University Cambridge MAUSA
                Author notes
                [* ] Corresponding author: Evan P. Economo, Okinawa Institute of Science and Technology Graduate University, 1919‐1 Tancha, Onna‐son, Okinawa 904‐0495, Japan.

                E‐mail: evaneconomo@ 123456gmail.com

                Article
                JBI12592
                10.1111/jbi.12592
                5014176
                © 2015 The Authors. Journal of Biogeography Published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution‐NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited and no modifications or adaptations are made.

                Page count
                Pages: 13
                Product
                Funding
                Funded by: NSF
                Award ID: DEB‐1145989
                Award ID: DEB‐0816749
                Award ID: DEB‐0515678
                Funded by: OIST
                Funded by: Ministry of Education and Science of the Russian Federation
                Award ID: 6.1933.2014/K
                Funded by: Czech Science Foundation
                Award ID: P505/12/2467
                Funded by: Marie Curie Fellowship
                Award ID: PIOFGA2009‐25448
                Categories
                Original Article
                All about Ants
                Custom metadata
                2.0
                jbi12592
                December 2015
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:09.09.2016

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