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      Which Factors Determine Spatial Segregation in the South American Opossums ( Didelphis aurita and D. albiventris)? An Ecological Niche Modelling and Geometric Morphometrics Approach

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          Abstract

          Didelphis albiventris and D. aurita are Neotropical marsupials that share a unique evolutionary history and both are largely distributed throughout South America, being primarily allopatric throughout their ranges. In the Araucaria moist forest of Southern Brazil these species are sympatric and they might potentially compete having similar ecology. For this reason, they are ideal biological models to address questions about ecological character displacement and how closely related species might share their geographic space. Little is known about how two morphologically similar species of marsupials may affect each other through competition, if by competitive exclusion and competitive release. We combined ecological niche modeling and geometric morphometrics to explore the possible effects of competition on their distributional ranges and skull morphology. Ecological niche modeling was used to predict their potential distribution and this method enabled us to identify a case of biotic exclusion where the habit generalist D. albiventris is excluded by the presence of the specialist D. aurita. The morphometric analyses show that a degree of shape discrimination occurs between the species, strengthened by allometric differences, which possibly allowed them to occupy marginally different feeding niches supplemented by behavioral shift in contact areas. Overlap in skull morphology is shown between sympatric and allopatric specimens and a significant, but weak, shift in shape occurs only in D. aurita in sympatric areas. This could be a residual evidence of a higher past competition between both species, when contact zones were possibly larger than today. Therefore, the specialist D. aurita acts a biotic barrier to D. albiventris when niche diversity is not available for coexistence. On the other hand, when there is niche diversification (e.g. habitat mosaic), both species are capable to coexist with a minimal competitive effect on the morphology of D. aurita.

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          Equilibrium of Global Amphibian Species Distributions with Climate

          A common assumption in bioclimatic envelope modeling is that species distributions are in equilibrium with contemporary climate. A number of studies have measured departures from equilibrium in species distributions in particular regions, but such investigations were never carried out for a complete lineage across its entire distribution. We measure departures of equilibrium with contemporary climate for the distributions of the world amphibian species. Specifically, we fitted bioclimatic envelopes for 5544 species using three presence-only models. We then measured the proportion of the modeled envelope that is currently occupied by the species, as a metric of equilibrium of species distributions with climate. The assumption was that the greater the difference between modeled bioclimatic envelope and the occupied distribution, the greater the likelihood that species distribution would not be at equilibrium with contemporary climate. On average, amphibians occupied 30% to 57% of their potential distributions. Although patterns differed across regions, there were no significant differences among lineages. Species in the Neotropic, Afrotropics, Indo-Malay, and Palaearctic occupied a smaller proportion of their potential distributions than species in the Nearctic, Madagascar, and Australasia. We acknowledge that our models underestimate non equilibrium, and discuss potential reasons for the observed patterns. From a modeling perspective our results support the view that at global scale bioclimatic envelope models might perform similarly across lineages but differently across regions.
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            Parallel evolution of character displacement driven by competitive selection in terrestrial salamanders

             Dean C Adams (2010)
            Background Parallel evolution can occur when common environmental factors exert similar selective forces on morphological variation in populations in different geographic localities. Competition can also generate morphological shifts, and if competing species co-occur in multiple geographic regions, then repeated instances of competitively-driven morphological divergence (character displacement) can occur. Despite the importance of character displacement for inferring the role of selection in morphological evolution however, replicated instances of sympatric morphological divergence are understudied. Results I tested the hypothesis that interspecific competition generated patterns of parallel morphological divergence in multiple geographic locations where two competing salamander species, Plethodon jordani and P. teyahalee, come into contact. I used geometric morphometrics to characterize head shape and found ecological character displacement in sympatric localities on each of three distinct mountains (geographic transects), where sympatric specimens displayed greater cranial differences and an increase in cranial robustness as compared to allopatric specimens. Using a recently developed analytical procedure, I also found that the observed morphological evolution within each species was consistent among transects; both in the total amount of morphological change as well as the direction of evolution in the morphological data space. This provided strong statistical evidence of parallel morphological evolution within species across replicate geographic transects. Conclusions The results presented here reveal that the morphological evolution of each species followed a common evolutionary path in each transect. Because dispersal between sympatric locations among transects is unlikely, these findings suggest that the repeated instances of character displacement have evolved in situ. They also suggest that selection from competitive interactions plays an important role in initiating sympatric morphological divergence in these species, and drives parallel sympatric morphological divergence between species.
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              Bergmann's rule across the equator: a case study in Cerdocyon thous (Canidae).

              1. The variation in cranial size of the crab-eating fox Cerdocyon thous was analysed in relation to latitude and several environmental variables throughout its distribution in South America. 2. We tested the existence of clines to determine whether this canid follows Bergmann's rule to the north and south of the Equator. Also, using niche modelling, we analysed whether the climatic changes during the last glaciation could have influenced Bergmann's rule in this species. We quantified the size of the cranium of C. thous (n = 300). The data were divided into two groups: (i) south of the Equator (n = 163) and (ii) north of the Equator (n = 137). We performed correlations, OLS regressions and simultaneous autoregressions to analyse the relationship between the variation in size and different geographic and environmental variables. Data of occurrence (n = 594) together with ambient variables from the present and the last glacial maximum (LGM) were used to predict the occurrence of C. thous with the implementation of the maximum entropy method. Present-day and historical distribution maps were obtained. 3. The variation in the size of the cranium of C. thous showed two trends. In the south of Equator, we observed that the size of the skull shows an inverse relationship with temperature-related variables and a positive one with precipitation, while in north of the Equator, we observed the opposite relationship. Populations south of the Equator follow Bergmann's rule showing increasing size with increasing latitude. To the north of the Equator, a non-Bergmannian pattern occurs because size decreases with increasing latitude. 4. Niche modelling showed two present-day groupings in South America, one north of Amazonia and the other south. However, for the period of the LGM, four groups emerged, possibly related to the four subspecies presently described for C. thous. Therefore, it is possible that the observed pattern - southern populations following Bergmann's rule while northern populations reflecting the opposite - has been influenced by the events that occurred during the LGM that could have led to the differentiation of populations.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                23 June 2016
                2016
                : 11
                : 6
                Affiliations
                [1 ]Laboratório de Ecologia e Biogeografia, Departamento de Ecologia e Evolução, Universidade Federal de Santa Maria, Santa Maria, Brazil
                [2 ]Laboratório de Ecologia Teórica e Síntese, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Goiânia, Brazil
                [3 ]Programa de Pós-Graduação em Ecologia e Conservação, CCBS, Universidade Federal do Mato Grosso do Sul, Campo Grande, Brazil
                [4 ]Research Centre in Evolutionary Anthropology and Palaeoecology, School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, England
                [5 ]Programa de Pós-Graduação em Biodiversidade Animal, CCNE, Universidade Federal de Santa Maria, Santa Maria, Brazil
                University of Naples, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NCC JMB MMW. Performed the experiments: MMW JMB. Analyzed the data: MMW JMB CM. Contributed reagents/materials/analysis tools: NCC MMW JS RSC GLM JMB CM. Wrote the paper: NCC MMW JS RSC GLM JMB CM.

                Article
                PONE-D-15-40431
                10.1371/journal.pone.0157723
                4919065
                27336371
                © 2016 Cáceres et al

                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.

                Page count
                Figures: 8, Tables: 1, Pages: 19
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award Recipient :
                Funded by: British Research Council
                Award ID: 127432108
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award Recipient :
                The contribution of Carlo Meloro to this research was supported by the British Research Council Travel grant (ref: 127432108). The senior author (Nilton Cáceres) was supported by the ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPq) in Brazil (PQ Researcher Fellow process number 308957/2010-5). Author Marcelo de Moraes Weber was supported by CNPq and Geruza Melo, Jonas Sponchiado, Renan Carvalho and Jamile Bubadué by ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior’ (CAPES) with a scholarship.
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