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Biogeography, cryptic diversity, and queen dimorphism evolution of the Neotropical ant genus Ectatomma Smith, 1958 (Formicidae, Ectatomminae)

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Due to its high biodiversity and its complex climatic and geological history, the Neotropical region has caught the attention of evolutionary and conservation biologists. The Neotropics have an understudied and probably extensive cryptic diversity, stemming from old lineages that have persisted through time with highly similar morphology or from new morphologically undifferentiated sibling species. The wide-ranging Neotropical ant genus Ectatomma currently has only 15 described species, some of which present limited distribution. These ants provide an excellent system for the study of diversification and cryptic diversity in the Neotropics. Ectatomma also displays queen-size dimorphism in some northern populations of its two most common species: a case of true microgyny and a recently described parasitic species. We performed a phylogenetic and biogeographic analysis of Ectatomma species using two mitochondrial genes and one nuclear gene. We also explored the relationship between the history of the genus and the appearance of miniaturized queens. Our analysis recovered a monophyletic Ectatomma that originated in the Parana region of South America. We recorded three likely events of colonization of the Caribbean-Mesoamerican region. We also detected ample evidence of cryptic divergence that deserves a full taxonomic revision of the genus. Miniature queens—microgynes and parasites—represent two independent evolutionary events that appeared in the recent history of the genus.
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... (Smith, 1936). Este gênero apresenta potencial para estudos evolutivos por apresentar tanto parasitismo social quanto microgínia (populações da mesma espécie com rainhas menores), que parecem ser eventos recentes na história evolutiva das espécies do gênero (Feitosa et al., 2008;Nettel-Hernanz et al., 2015). Na ESEC do Rio Ronuro o gênero foi amostrado na vegetação e no solo. ...
... However, the distribution of Ectatomma tuberculatum (Olivier, 1792) extends to Texas, in the EUA (Smith, 1936). This genus presents potential for evolutionary studies because it presents both social parasitism and microgynia (populations of the same species with smaller queens), which appear to be recent events in the evolutionary history of species of the genus (Feitosa et al., 2008;Nettel-Hernanz et al., 2015). At Rio Ronuro ESEC, the genus was sampled in vegetation and soil. ...
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This study presents a preliminary inventory of butterflies (Lepidoptera: Papilionoidea) in the Rio Ronuro Ecological Station in Brazil. Butterflies were sampled in eight plots dis�tributed in three sites located between the Municipality of Nova Ubiratã and Paranatin�ga and Santiago do Norte. We sampled 30 species of butterflies, in four families, Nymph�alidae, Pieridae, Papilionidae e Riodinidae. The sampling period was short and lacking temporal repetitions, however considering the low numbers of traps installed (36) and sampling during the rainy season our results indicate a large potential diversity of butter�flies to be explored in the future in the station.
... (Smith, 1936). Este gênero apresenta potencial para estudos evolutivos por apresentar tanto parasitismo social quanto microgínia (populações da mesma espécie com rainhas menores), que parecem ser eventos recentes na história evolutiva das espécies do gênero (Feitosa et al., 2008;Nettel-Hernanz et al., 2015). Na ESEC do Rio Ronuro o gênero foi amostrado na vegetação e no solo. ...
... However, the distribution of Ectatomma tuberculatum (Olivier, 1792) extends to Texas, in the EUA (Smith, 1936). This genus presents potential for evolutionary studies because it presents both social parasitism and microgynia (populations of the same species with smaller queens), which appear to be recent events in the evolutionary history of species of the genus (Feitosa et al., 2008;Nettel-Hernanz et al., 2015). At Rio Ronuro ESEC, the genus was sampled in vegetation and soil. ...
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Arthropods are important components of edaphic environments, being responsible for numerous processes related to the decomposition and cycling of matter. Studies on their diversity are important for understanding the ecosystem dynamics. This study aimed to evaluate the composition of the edaphic community of arthropods, mainly arachnids, in a Cerrado-Amazônia transition area at the Rio Ronuro Ecological Station, in Nova Ubiratã, Mato Grosso. Arthropods were sampled in October/November 2016 and in February/March 2017, using pitfall traps. Opiliones were collected manually. As a result 9,611 arthropods were obtained, distributed among Hexapoda, Arachnida, Diplopoda and Chilopoda and 21 taxonomic orders. Hymenoptera (4,984 ind.; 51.9%), Diptera (2,299 ind.; 23.9%), Collembola (660 ind.; 6.9%), Isoptera (581 ind.; 6%) and Coleoptera (435 ind.; 4.5%) predominated. Among the spiders (220 ind.; 2.3%) were identified 24 families and nine behavioral guilds. Zodariidae (60 ind.; 28%), Lycosidae (51 ind.; 22%) and Theridiidae (32 ind.; 14%) predominated. The Opiliones (15 ind.; 0.2%) were Cosmetidae (10 ind.; 66.6%), Stygnidae (3 ind.; 20%) and Manaosbiidae (2 ind.; 13.4%). The results indicate that Rio Ronuro ESEC presents considerable edaphic biodiversity, corroborating its importance as an area for the conservation of Southern Amazonia.
... (Smith, 1936). Este gênero apresenta potencial para estudos evolutivos por apresentar tanto parasitismo social quanto microgínia (populações da mesma espécie com rainhas menores), que parecem ser eventos recentes na história evolutiva das espécies do gênero (Feitosa et al., 2008;Nettel-Hernanz et al., 2015). Na ESEC do Rio Ronuro o gênero foi amostrado na vegetação e no solo. ...
... However, the distribution of Ectatomma tuberculatum (Olivier, 1792) extends to Texas, in the EUA (Smith, 1936). This genus presents potential for evolutionary studies because it presents both social parasitism and microgynia (populations of the same species with smaller queens), which appear to be recent events in the evolutionary history of species of the genus (Feitosa et al., 2008;Nettel-Hernanz et al., 2015). At Rio Ronuro ESEC, the genus was sampled in vegetation and soil. ...
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With a territory of 90,680,600 hectares, the state of Mato Grosso possesses a broad range of natural beauty and rich biodiversity and currently houses 46 state conservation units that encompass 3.2 million hectares. A significant part of this biodiversity, however, remains un�known due to limited knowledge generation and dissemination. Rio Ronuro Ecological Station is one of five existing state ecological stations in Mato Grossso. It stands out for being located in the central region of the state, specifically comprising the transition between the Cerrado and Amazonia biomes (area with Savanna/Seasonal Forest/Ombrophilous Forest), bestowing it with the potential to harbor rich biodiversity and thus unique relevance within State System of Conservation Units. In compliance with the objective for which Rio Ronuro Ecological Station was created – protection of existing ecosystems, development of scientific research and conservation ed�ucation – State Secretary of Environment of Mato Grosso (SEMA-MT), together with the technical cooperation of Amazon Region Protected Areas Program (ARPA) and researchers of Federal University of Mato Grosso (UFMT), and support from Biodiversity Research Pro�gram (PPBIO), contributed efforts to survey and catalog the station’s flora and fauna. Scientific research developed in the conservation unit has broadened knowledge of biodiver�sity, provided training for students and local community agents, encouraged bioprospecting studies of species with potential that occur in the region, and made this publication possi�ble, which brings together all the systematic studies carried out to date. The knowledge gathered in this work will contribute to the processes of environmental edu�cation and conservation of biodiversity, as well as provide academic information for society in general. This knowledge will support the decision-making process for public policies for Rio Ronuro Ecological Station, enable its valorization and acknowledge the ecological pro�cesses that maintain it. Mauren Lazzaretti Mato Grosso State Secretary of the Environment
... (Smith, 1936). Este gênero apresenta potencial para estudos evolutivos por apresentar tanto parasitismo social quanto microgínia (populações da mesma espécie com rainhas menores), que parecem ser eventos recentes na história evolutiva das espécies do gênero (Feitosa et al., 2008;Nettel-Hernanz et al., 2015). Na ESEC do Rio Ronuro o gênero foi amostrado na vegetação e no solo. ...
... However, the distribution of Ectatomma tuberculatum (Olivier, 1792) extends to Texas, in the EUA (Smith, 1936). This genus presents potential for evolutionary studies because it presents both social parasitism and microgynia (populations of the same species with smaller queens), which appear to be recent events in the evolutionary history of species of the genus (Feitosa et al., 2008;Nettel-Hernanz et al., 2015). At Rio Ronuro ESEC, the genus was sampled in vegetation and soil. ...
Chapter
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Os macrofungos têm sido pouco estudados nos diferentes biomas brasileiros e estima-se que há muitas espécies ainda a serem descritas. Este capítulo apresenta um levantamento incluindo a descrição de dezesseis espécies de Basidomycota (cogumelos lamelares e fungos clavarioides) coletados na Estação Ecológica do Rio Ronuro, Mato Grosso. Para cada espécie são apresentados dados taxonômicos e de distribuição geográfica no Brasil. Dez espécies são registradas pela primeira vez para o estado do Mato Grosso.
... Hence, when the Typical Neotropical cenocron is analysed, the oldest part of the history is not included in all cases, but in most cases only the recent clades in a phylogeny are considered. Another situation occurred with the ants Eciton and Ectatomma, which have had several dispersal events to Central America since the Late Miocene (Nettel-Hernanz et al., 2015;Winston et al., 2017), and their low vagility has promoted parapatric speciation showing a pattern of parallel evolution (Winston et al., 2017). ...
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Analysis of the biotic assembly of the Mexican Transition Zone (MTZ) is challenging because of the convergence of taxa with different origins and biogeographical histories. The typical Neotropical cenocron corresponds to genera widespread in South America that might have dispersed to the MTZ in the Pliocene–Holocene. It has been exemplified with distributional patterns of several plant and animal taxa; however, their historical congruence has not been tested. We examined the historical relationships among the areas of endemism where Typical Neotropical taxa are found through a cladistic biogeographical analysis to determine whether they have dispersed simultaneously, showing a geodispersal pattern. We searched for Neotropical clades that dispersed to the MTZ from the Pliocene to the present. The distribution of nine animal clades in seven areas of endemism was analysed by cladistic biogeography. Redundant areas and widespread taxa were treated with paralogy-free and transparent methods. Patterns of area relationships were searched using a parsimony analysis of paralogy-free subtrees. The parsimony analysis found a single resolved tree showing a general pattern of area relationships: (Chacoan ((South Brazilian (Boreal Brazilian + Lesser Antilles)), (South American Pacific (Mesoamerican-Central America + Western Mexico)))). Distributional and phylogenetic information on the groups analysed contrast with a previous cladistic biogeographical analysis that has shown different area relationships, thus supporting the general hypothesis of a geodispersal event of the Typical Neotropical cenocron in the MTZ. Additionally, the analysis provided evidence of vicariant events related to the lifting of the Northern Andes and climatic changes during the Pleistocene.
... Consequently, two competing hypotheses were developed for explaining the speciation mechanisms of social parasites: 1) The interspecific hypothesis proposes that host and social parasite evolved reproductive isolation in allopatry, whereas 2) the intraspecific hypothesis postulates that the social parasite evolved directly from its host in sympatry (3,13,18,20,21,(31)(32)(33)(34)(35)(36)(37). Empirical studies of temporary, dulotic, and host queen-intolerant workerless ant social parasites generally provide support for the interspecific hypothesis (14,(38)(39)(40)(41)(42)(43)(44)(45)(46)(47)(48), whereas recent phylogenetic studies lend support to the intraspecific hypothesis for queentolerant inquilines (33,36,(49)(50)(51). In some cases, host shifts, secondary speciation events of hosts and/or parasites, and extinctions obscure the original evolutionary conditions under which social parasitism originated (52)(53)(54). ...
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Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 172 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed a global phylogeny of Formica ants. The genus originated in the Old World ∼30 Ma ago and dispersed multiple times to the New World and back. Within Formica , obligate dependent colony-founding behavior arose once from a facultatively polygynous common ancestor practicing independent and facultative dependent colony foundation. Temporary social parasitism likely preceded or arose concurrently with obligate dependent colony founding, and dulotic social parasitism evolved once within the obligate dependent colony-founding clade. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from a facultative parasitic background in socially polymorphic organisms. In contrast to permanently socially parasitic ants in other genera, the high parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.
... In general, inquiline social parasites are of interest to evolutionary biology because of their departures from a free-living life history, the convergent morphological and behavioral evolution of traits associated with the socially parasitic life history, as well as their close phylogenetic relationships to their hosts. Previous studies revealed that some inquiline species evolved directly from their host species via sympatric speciation (Savolainen and Vepsäläinen 2003;Rabeling et al. 2014;Leppänen et al. 2015;Nettel-Hernanz et al. 2015) whereas other inquilines likely originated in allopatry (Agosti 1994;Sanetra and Buschinger 2000;Ward et al. 2015). In a forthcoming study, we will test whether Nylanderia inquilines evolved via the intra-or the interspecific route of social parasite evolution. ...
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In ants, social parasitism is an umbrella term describing a variety of life-history strategies, where a parasitic species depends entirely on a free-living species, for part of or its entire life-cycle, for either colony founding, survival, and/or reproduction. The highly specialized inquiline social parasites are fully dependent on their hosts for their entire lifecycles. Most inquiline species are tolerant of the host queen in the parasitized colony, forgo producing a worker caste, and invest solely in the production of sexual offspring. In general, inquilines are rare, and their geographic distribution is limited, making it difficult to study them. Inquiline populations appear to be small, cryptic, and they are perhaps ephemeral. Thus, information about their natural history is often fragmentary or non-existent but is necessary for understanding the socially parasitic life history syndrome in more detail. Here, we describe two new species of inquiline social parasites, Nylanderia deyrupisp. nov. and Nylanderia parasiticasp. nov. , from the southeastern United States, parasitizing Nylanderia wojciki and Nylanderia faisonensis , respectively. The formicine genus Nylanderia is large and globally distributed, but until the recent description of Nylanderia deceptrix , social parasites were unknown from this genus. In addition to describing the new social parasite species, we summarize the fragmentary information known about their biology, present a key to both the queens and the males of the Nylanderia social parasites, and discuss the morphology of the social parasites in the context of the inquiline syndrome.
Thesis
To describe and understand biodiversity, the identification of species is essential. Because some species diversify without revealing any morphologic change, the use of different taxonomic tools is highly recommended. Among the advantages of employing different traits for species classification, one of the most remarkable is that at the same time we obtain information about which traits have been involved in the diversification of species. In this study I investigated the variation observed in the ant species Ectatomma ruidum as an evidence of different taxa. E. ruidum is a widely distributed ant from the Neotropics and in previous studies based on mitochondrial sequences the species was proposed to include at least four different taxa. The geographic distribution patterns of the putative species shows that some of them are restricted to small areas, without any apparent geographic barrier separating populations, which raised the question about which mechanisms separated them. By analyzing recognition cues, acoustic signals, morphological acoustic traits and DNA sequences (mitochondrial DNA COI gene, 3RAD and UCE) I provide evidence supporting the separation for most of the previously proposed species. Additionally, the combination of phenotypic and genetic information unveiled that recognition cues may have had a very important role in the diversification of the species complex. Overall, this study adds evidence in favor of the use of a multi trait approach for the delimitation of closely related specie
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Uncovering the evolutionary history of the subfamilies Ectatomminae and Heteroponerinae, or ectaheteromorphs, is key to understanding a major branch of the ant tree of life. Despite their diversity and ecological importance, phylogenetic relationships in the group have not been well explored. One particularly suitable tool for resolving phylogeny is the use of ultraconserved elements (UCEs), which have been shown to be ideal markers at a variety of evolutionary time scales. In the present study, we enriched and sequenced 2,127 UCEs from 135 specimens of ectaheteromorph ants and investigated phylogeny using a variety of model-based phylogenomic methods. Trees recovered from partitioned maximum-likelihood and species-tree analyses were well resolved and largely congruent. The results are consistent with an expanded concept of Ectatomminae that now includes the subfamily Heteroponerinae new synonym and its single tribe Heteroponerini new combination. Eleven monophyletic groups are recognized as genera: Acanthoponera, Alfariastatus revived, Boltonia Camacho and Feitosa new genus, Ectatomma, Gnamptogenys, Heteroponera, Holcoponerastatus revived, Poneracanthastatus revived, Rhytidoponera, Stictoponerastatus revived, and Typhlomyrmex. The new phylogenetic framework and classification proposed here will shed light on the study of Ectatomminae taxonomy and systematics, as well as on the morphological evolution of the groups that it comprises.
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Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 178 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life-history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed the first global phylogeny of Formica ants and representative formicine outgroups. The genus Formica originated in the Old World during the Oligocene (~30 Ma ago) and dispersed multiple times to the New World. Within Formica, the capacity for dependent colony foundation and temporary social parasitism arose once from a facultatively polygynous, independently colony founding ancestor. Within this parasitic clade, dulotic social parasitism evolved once from a facultatively temporary parasitic ancestor that likely practiced colony budding frequently. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from different facultative parasitic backgrounds in socially polymorphic organisms. In contrast to inquiline ant species in other genera, the high social parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.
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