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  • 1. Araujo, Sabrina B. L.
    et al.
    Braga, Mariana Pires
    Universidade Federal do Paraná, Brazil.
    Brooks, Daniel R.
    Agosta, Salvatore J.
    Hoberg, Eric P.
    von Hartenthal, Francisco W.
    Boeger, Walter A.
    Understanding host-switching by ecological fitting2015In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 10, no 10, article id e0139225Article in journal (Refereed)
    Abstract [en]

    Despite the fact that parasites are highly specialized with respect to their hosts, empirical evidence demonstrates that host switching rather than co-speciation is the dominant factor influencing the diversification of host-parasite associations. Ecological fitting in sloppy fitness space has been proposed as a mechanism allowing ecological specialists to host-switch readily. That proposal is tested herein using an individual-based model of host switching. The model considers a parasite species exposed to multiple host resources. Through time host range expansion can occur readily without the prior evolution of novel genetic capacities. It also produces non-linear variation in the size of the fitness space. The capacity for host colonization is strongly influenced by propagule pressure early in the process and by the size of the fitness space later. The simulations suggest that co-adaptation may be initiated by the temporary loss of less fit phenotypes. Further, parasites can persist for extended periods in sub-optimal hosts, and thus may colonize distantly related hosts by a "stepping-stone" process.

  • 2. Boeger, Walter A.
    et al.
    Marteleto, Flávio M.
    Zagonel, Letícia
    Braga, Mariana P.
    Universidade Federal do Paraná, Brazil.
    Tracking the history of an invasion: the freshwater croakers (Teleostei: Sciaenidae) in South America2015In: Zoologica Scripta, ISSN 0300-3256, E-ISSN 1463-6409, Vol. 44, no 3, p. 250-262Article in journal (Refereed)
    Abstract [en]

    In this study, the competing hypotheses of single vs. double colonisation events for freshwater Pachyurinae (Sciaenidae) in South America is tested and the historical biogeography of the expansion of this clade within the continent is reconstructed based on phylogenetic analysis. Parsimony and Bayesian inference (BI) for 19 marine and freshwater species assigned to Sciaenidae, Haemulidae and Polypteridae were determined based on partial sequences of the mitochondrial 16S and cytochrome b genes and fragments of the nuclear Tmo-4C4 and rhodopsin genes. A parsimonious ancestral character reconstruction of euryhalinity was performed on a clade of families of closely related fishes to evaluate the role of ecological fitting in the colonisation of freshwater by a marine sciaenid. The parsimony and BI phylogenetic hypotheses for the concatenated sequences supported the monophyly of the freshwater Sciaenidae. Divergence of the two freshwater clades of Sciaenidae, Pachyurinae and Plagioscion, occurred within the Amazon Basin. Within Pachyurinae, two clades were recovered: one composed of species from the Amazon and the Paraná Basin and a second with representatives from the São Francisco and south-eastern Atlantic basins. The results were compatible with the hypothesis of a single colonisation event of South American freshwater habitats by a marine lineage. The hypothesis of gradual adaptation to freshwater was rejected in favour of the hypothesis of ecological fitting. Sciaenidae, or a subordinate lineage within the family, is ancestrally capable of withstanding exposure to low-salinity habitats, which putatively facilitated the colonisation of freshwater habitats. The subsequent diversification and expansion of Pachyurinae across South America followed this colonisation and replicated the general pattern of the area relationships of South American river basins for several other fish groups.

  • 3.
    Braga, Mariana P.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Araujo, Sabrina B. L.
    Agosta, Salvatore
    Brooks, Daniel
    Hoberg, Eric
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Janz, Niklas
    Stockholm University, Faculty of Science, Department of Zoology.
    Boeger, Walter A.
    Host use dynamics in a heterogeneous fitness landscape generates oscillations in host range and diversification2018In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 72, no 9, p. 1773-1783Article in journal (Refereed)
    Abstract [en]

    Colonization of novel hosts is thought to play an important role in parasite diversification, yet little consensus has been achieved about the macroevolutionary consequences of changes in host use. Here, we offer a mechanistic basis for the origins of parasite diversity by simulating lineages evolved in silico. We describe an individual-based model in which (i) parasites undergo sexual reproduction limited by genetic proximity, (ii) hosts are uniformly distributed along a one-dimensional resource gradient, and (iii) host use is determined by the interaction between the phenotype of the parasite and a heterogeneous fitness landscape. We found two main effects of host use on the evolution of a parasite lineage. First, the colonization of a novel host allowed parasites to explore new areas of the resource space, increasing phenotypic and genotypic variation. Second, hosts produced heterogeneity in the parasite fitness landscape, which led to reproductive isolation and therefore, speciation. As a validation of the model, we analyzed empirical data from Nymphalidae butterflies and their host plants. We then assessed the number of hosts used by parasite lineages and the diversity of resources they encompass. In both simulated and empirical systems, host diversity emerged as the main predictor of parasite species richness.

  • 4.
    Braga, Mariana P.
    et al.
    Universidade Federal do Paraná, Brazil.
    Araujo, Sabrina B. L.
    Universidade Federal do Paraná, Brazil.
    Boeger, Walter A.
    Universidade Federal do Paraná, Brazil.
    Patterns of interaction between Neotropical freshwater fishes and their gill Monogenoidea (Platyhelminthes)2014In: Parasitology Research, ISSN 0932-0113, E-ISSN 1432-1955, Vol. 113, no 2, p. 481-490Article in journal (Refereed)
    Abstract [en]

    Using network analysis, we looked for broad patterns of distribution of Monogenoidea gill parasites on Neotropical freshwater fishes within a host phylogenetic framework. We analyzed a database of Monogenoidea parasitizing fishes from Neotropical rivers, from 23 watersheds, based on species descriptions published until 2011. Host–parasite interactions were organized into five matrices grouping species at different taxonomic levels. The network of interactions between host families and parasite genera was significantly modular and revealed that each fish order has a unique composition of parasite genera. Hence, interactions between lower taxa were analyzed separately for the largest fish orders (Perciformes, Siluriformes, and Characiformes). Networks tended to be loosely connected and organized in modules. Despite the putative high host specificity of monogenoids, some have a wider host range that includes distantly related host species. Among the hosts, the clade composed by the piranhas (Serrasalmus spp. and related species, Serrasalmidae) stands out in terms of parasite richness per host species, resulting in a more connected network. The history of the lineages of each host order within Neotropical freshwaters seems to have a great influence on the extent of parasite sharing. The observed modularity was influenced by both spatial structure and phylogenetic relatedness of species. In average, 37 % of modules of networks between host species and parasite genera were associated with a particular river basin and 63 % of modules were associated with a host family. Hence, spatial structure determines the co-occurrence of host and parasite species, but their evolutionary history is the main factor defining which interactions are possible.

  • 5.
    Braga, Mariana P.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Guimarães Jr, Paulo R.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Janz, Niklas
    Stockholm University, Faculty of Science, Department of Zoology.
    Unifying host-associated diversification processes using butterfly-plant networks2018In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 9, article id 5155Article in journal (Refereed)
    Abstract [en]

    Explaining the exceptional diversity of herbivorous insects is an old problem in evolutionary ecology. Here we focus on the two prominent hypothesised drivers of their diversification, radiations after major host switch or variability in host use due to continuous probing of new hosts. Unfortunately, current methods cannot distinguish between these hypotheses, causing controversy in the literature. Here we present an approach combining network and phylogenetic analyses, which directly quantifies support for these opposing hypotheses. After demonstrating that each hypothesis produces divergent network structures, we then investigate the contribution of each to diversification in two butterfly families: Pieridae and Nymphalidae. Overall, we find that variability in host use is essential for butterfly diversification, while radiations following colonisation of a new host are rare but can produce high diversity. Beyond providing an important reconciliation of alternative hypotheses for butterfly diversification, our approach has potential to test many other hypotheses in evolutionary biology.

  • 6.
    Braga, Mariana P.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Landis, Michael
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Janz, Niklas
    Stockholm University, Faculty of Science, Department of Zoology.
    Ronquist, Fredrik
    Bayesian analysis of host repertoire evolutionManuscript (preprint) (Other academic)
  • 7.
    Braga, Mariana P.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Landis, Michael
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Janz, Niklas
    Stockholm University, Faculty of Science, Department of Zoology.
    Ronquist, Fredrik
    Evolution of butterfly-plant networks revealed by Bayesian inference of host repertoireManuscript (preprint) (Other academic)
  • 8.
    Braga, Mariana P
    et al.
    Universidade Federal do Paraná, Brazil.
    Razzolini, Emanuel
    Universidade Federal do Paraná, Brazil.
    Boeger, Walter A.
    Universidade Federal do Paraná, Brazil.
    Drivers of parasite sharing among Neotropical freshwater fishes2015In: Journal of Animal Ecology, ISSN 0021-8790, E-ISSN 1365-2656, Vol. 84, no 2, p. 487-497Article in journal (Refereed)
  • 9.
    Braga, Mariana Pires
    Stockholm University, Faculty of Science, Department of Zoology.
    Evolution of host repertoires and the diversification of butterflies2019Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    All herbivorous insects are specialized to some extent to their host plants, but the level of specialization varies greatly. Insect-plant coevolution is often invoked to explain the large diversity of herbivorous insects, but the role of specialization during diversification is still controversial. Although well-studied, our understanding of the evolution of species interactions is still improving, and recent theoretical developments have highlighted the role of generalization (via colonization of new hosts) on diversification. In this thesis, various approaches are combined for a detailed study of the origins of macroevolutionary patterns of host use and butterfly diversity. Chapter I provides a mechanistic basis for such patterns through simulations of lineages evolved in silico. By separating the effects of the number of hosts used by a parasite lineage and the diversity of resources they encompass, we found that resource diversity, rather than host range per se, was the main driver of parasite species richness in both simulated and empirical systems. In Chapter II, we combined network and phylogenetic analyses to quantify support for the two main hypothesized drivers of diversification of herbivorous insects. Based on analyses of two butterfly families, Nymphalidae and Pieridae, we found that variability in host use is essential for diversification, while radiation following the colonization of a new host is rare but can produce high diversity. We then reconciled the two alternative hypotheses into a unified process of host-associated diversification where continuous probing of new hosts and retention of the ability to use hosts colonized in the past are the main factors shaping butterfly-plant networks. While network analysis is a powerful tool for investigating patterns of interaction, other methods are necessary to directly test the mechanisms generating the observed patterns. Therefore, in Chapter III we describe a model of host repertoire evolution we developed for Bayesian inference of evolution of host-parasite interactions. The approach was validated with both simulated and empirical data sets. Finally, in Chapter IV we used the method described in Chapter III to explicitly test the predictions made in Chapter II about the evolution of butterfly-plant networks. We found direct evidence for the role of expansion of fundamental host repertoire and phylogenetic conservatism as important drivers of host repertoire evolution. Thus, using three different approaches, we found overall support for the idea that variation in host use accumulated over evolutionary time is essential for butterfly diversification.

  • 10.
    Janz, Niklas
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Braga, Mariana P
    Stockholm University, Faculty of Science, Department of Zoology.
    Wahlberg, Niklas
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    On oscillations and flutterings - A reply to Hamm and Fordyce2016In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 5, p. 1150-1155Article in journal (Refereed)
    Abstract [en]

    The diversification of plant-feeding insects is seen as a spectacular example of evolutionary radiation. Hence, developing hypotheses to explain this diversification, and methods to test them, is an important undertaking. Some years ago, we presented the oscillation hypothesis as a general process that could drive diversification of this and similar interactions, through repeated expansions and contractions of host ranges. Hamm and Fordyce recently presented a study with the outspoken intention of testing this hypothesis where they concluded that the oscillation hypothesis was not supported. We point out several problems with their study, owing both to a misrepresentation of our hypothesis and to the methods. We provide a clarifying description of the oscillation hypothesis, and detail some predictions that follow from it. A reanalysis of the data demonstrated a troubling sensitivity of the "SSE" class of models to small changes in model specification, and we caution against using them for tests of trait-based diversification. Future tests of the hypothesis also need to better acknowledge the processes behind the host range oscillations. We suspect that doing so will resolve some of the apparent conflicts between our hypothesis and the view presented by Hamm and Fordyce.

  • 11.
    Nylin, Sören
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Agosta, Salvatore
    Bensch, Staffan
    Boeger, Walter A.
    P. Braga, Mariana
    Stockholm University, Faculty of Science, Department of Zoology.
    Brooks, Daniel R.
    Forister, Matthew L.
    Hambäck, Peter A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Hoberg, Eric P.
    Nyman, Tommi
    Schäpers, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    Stigall, Alycia L.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Österling, Martin
    Janz, Niklas
    Stockholm University, Faculty of Science, Department of Zoology.
    Embracing Colonizations: A New Paradigm for Species Association Dynamics2018In: Trends in Ecology & Evolution, ISSN 0169-5347, E-ISSN 1872-8383, Vol. 33, no 1, p. 4-14Article, review/survey (Refereed)
    Abstract [en]

    Parasitehost and insectplant research have divergent traditions despite the fact that most phytophagous insects live parasitically on their host plants. In parasitology it is a traditional assumption that parasites are typically highly specialized; cospeciation between parasites and hosts is a frequently expressed default expectation. Insectplant theory has been more concerned with host shifts than with cospeciation, and more with hierarchies among hosts than with extreme specialization. We suggest that the divergent assumptions in the respective fields have hidden a fundamental similarity with an important role for potential as well as actual hosts, and hence for host colonizations via ecological fitting. A common research program is proposed which better prepares us for the challenges from introduced species and global change.

  • 12.
    Rocha, Rosana M.
    et al.
    Universidade Federal do Paraná, Brasil.
    Cangussu, Leonardo C.
    Universidade Federal do Paraná, Brasil.
    Braga, Mariana P.
    Universidade Federal do Paraná, Brasil.
    Stationary substrates facilitate bioinvasion in paranaguá Bay in Southern Brazil2010In: Brazilian Journal of Oceanography, ISSN 1679-8759, E-ISSN 1982-436X, Vol. 58, no 3, p. 23-28Article in journal (Refereed)
    Abstract [en]

    Artificial substrates in and near ports and marinas commonly have many non-indigenous species andare the first stepping stone for the establishment of bioinvasors. Substrate movement influencesfouling communities and so understanding of how species assemblages are related to specificsubstrate conditions is crucial as a management tool. Here we describe the species assemblage of thecommunity after six months of development on granite plates in Paranaguá Bay. Species richnesswas similar in the two treatments, with 12 species on floating (constant depth) plates and 15 onstationary (variable depth) plates. However, species composition differed, with the community onfloating plates being dominated by the native bivalve Mytella charruana (66.1 + 5.5% cover) andthat on stationary plates dominated by the barnacles Fistulobalanus citerosum (49.8 + 3.5% cover)and the introduced Amphibalanus reticulatus (33.9 + 3.7% cover). Other introduced species wereGarveia franciscana, on one stationary plate, and Megabalanus coccopoma also on one stationaryplate and not very abundant on half of the floating plates (< 2%). Thus, stationary plates were moresusceptible to introduced species that may become very abundant, suggesting that this type ofsubstrate should be a priority in management for bioinvasion control. We also hypothesize that thenative bivalve M. charruana is the dominant competitor for space on floating substrates, therebyreducing the invasiveness of that type of substrate.

  • 13. Wang, Houshuai
    et al.
    Holloway, Jeremy D.
    Janz, Niklas
    Stockholm University, Faculty of Science, Department of Zoology.
    Braga, Mariana P.
    Stockholm University, Faculty of Science, Department of Zoology.
    Wahlberg, Niklas
    Wang, Min
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology.
    Polyphagy and diversification in tussock moths: Support for the oscillation hypothesis from extreme generalists2017In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 7, no 19, p. 7975-7986Article in journal (Refereed)
    Abstract [en]

    Theory on plasticity driving speciation, as applied to insect-plant interactions (the oscillation hypothesis), predicts more species in clades with higher diversity of host use, all else being equal. Previous support comes mainly from specialized herbivores such as butterflies, and plasticity theory suggests that there may be an upper host range limit where host diversity no longer promotes diversification. The tussock moths (Erebidae: Lymantriinae) are known for extreme levels of polyphagy. We demonstrate that this system is also very different from butterflies in terms of phylogenetic signal for polyphagy and for use of specific host orders. Yet we found support for the generality of the oscillation hypothesis, in that clades with higher diversity of host use were found to contain more species. These clades also consistently contained the most polyphagous single species. Comparing host use in Lymantriinae with related taxa shows that the taxon indeed stands out in terms of the frequency of polyphagous species. Comparative evidence suggests that this is most probably due to its nonfeeding adults, with polyphagy being part of a resulting life history syndrome. Our results indicate that even high levels of plasticity can drive diversification, at least when the levels oscillate over time.

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