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Obligatory ant–plant symbioses often appear to be single evolutionary shifts within particular ant lineages; however, convergence can be revealed once natural history observations are complemented with molecular phylogenetics. Here, we describe a remarkable example of convergent evolution in an ant–plant symbiotic system. Exclusively arboreal,Myrmelachistaspecies can be generalized opportunists nesting in several plant species or obligately symbiotic, live-stem nesters of a narrow set of plant species. Instances of specialization withinMyrmelachistaare known from northern South America and throughout Middle America. In Middle America, a diverse radiation of specialists occupies understory treelets of lowland rainforests. The morphological and behavioural uniformity of specialists suggests that they form a monophyletic assemblage, diversifying after a single origin of specialization. Using ultraconserved element phylogenomics and ancestral state reconstructions, we show that shifts from opportunistic to obligately symbiotic evolved independently in South and Middle America. Furthermore, our analyses support a remarkable case of convergence within the Middle American radiation, with two independently evolved specialist clades, arising nearly simultaneously from putative opportunistic ancestors during the late Pliocene. This repeated evolution of a complex phenotype suggests similar mechanisms behind trait shifts from opportunists to specialists, generating further questions about the selective forces driving specialization.

 

Comparative genomic studies of social insects suggest that changes in gene regulation are associated with evolutionary transitions in social behavior, but the activity of predicted regulatory regions has not been tested empirically. We used STARR-seq, a high-throughput enhancer discovery tool, to identify and measure the activity of enhancers in the socially variable sweat bee,Lasioglossum albipes. We identified over 36,000 enhancers in theL. albipesgenome from three social and three solitary populations. Many enhancers were identified in only a subset ofL. albipespopulations, revealing rapid divergence in regulatory regions within this species. Population-specific enhancers were often proximal to the same genes across populations, suggesting compensatory gains and losses of regulatory regions may preserve gene activity. We also identified 1182 enhancers with significant differences in activity between social and solitary populations, some of which are conserved regulatory regions across species of bees. These results indicate that social trait variation inL. albipesis driven both by the fine-tuning of ancient enhancers as well as lineage-specific regulatory changes. Combining enhancer activity with population genetic data revealed variants associated with differences in enhancer activity and identified a subset of differential enhancers with signatures of selection associated with social behavior. Together, these results provide the first empirical map of enhancers in a socially flexible bee and highlight links between cis-regulatory variation and the evolution of social behavior.

 

Abstract Coloration is an important phenotypic trait for taxonomic studies and has been widely used for identifying insect species and populations. However, coloration can be a poor diagnostic character for insect species that exhibit high polymorphism in this trait, which can lead to over-splitting of taxonomic units. In orchid bees, color variation has been interpreted by different taxonomists as either polymorphism associated with Müllerian mimicry complexes or diagnostic traits for species identification. Despite this uncertainty, integrative approaches that incorporate multiple independent datasets to test the validity of hair coloration as a character that identifies independent evolutionary units have not been used. Here, we use phylogenomic data from Ultraconserved Elements (UCEs) to explore whether color phenotypes in the widespread orchid bee species complexes Eulaema meriana and Eulaema bombiformis (Hymenoptera: Apidae: Euglossini) correspond to independent lineages or polymorphic trait variation within species. We find that lineages within both species are structured according to geography and that color morphs are generally unassociated with evolutionarily independent groups except for populations located in the Atlantic Forest of Brazil. We conclude that there is compelling evidence that E. atleticana and E. niveofasciata are subspecies of E. meriana and E. bombiformis, respectively, and not different species as previously suggested. Therefore, we recognize Eulaema meriana atleticanacomb. n. and Eulaema bombiformis niveofasciatacomb. n. and discuss their morphological characteristics. We make recommendations on the use of color traits for orchid bee taxonomy and discuss the significance of subspecies as evolutionary units relevant for conservation efforts. 

Species delimitation is a rich scientific field that often uses different sources of data to identify independently evolving lineages that might be recognized as species. Here, we use an integrative approach based on morphometrics, COI-barcoding, and phylogenomics using ultraconserved elements (UCEs) to investigate whether the orchid bee species Eulaema cingulata (Fabricius, 1804) and E. pseudocingulata Oliveira, 2006 represent a single variable taxon or two different species. We analyzed 126 specimens across the geographical range of these nominal species to test species hypotheses using the general lineage concept. We found substantial overlap in wing and head morphometrics, and both taxa form one phylogenetic lineage based on COI mitochondrial and UCE data. Our results support the recognition of both forms as members of the same evolutionary unit and E. pseudocingulata is herein recognized as a junior synonym of E. cingulata . 

Abstract The genus Cryptopone Emery contains 25 species of litter and soil ants, 5 of which occur in the Americas. Cryptopone gilva (Roger) occurs in the southeastern United States and cloud forests of Mesoamerica, exhibiting an uncommon biogeographic disjunction observed most often in plants. We used phylogenomic data from ultraconserved elements (UCEs), as well as mitogenomes and legacy markers, to investigate phylogenetic relationships, species boundaries, and divergence dates among New World Cryptopone. Species delimitation was conducted using a standard approach and then tested using model-based molecular methods (SNAPP, BPP, SODA, and bPTP). We found that Cryptopone as currently constituted is polyphyletic, and that all the South American species belong to Wadeura Weber, a separate genus unrelated to Cryptopone. A single clade of true Cryptopone occurs in the Americas, restricted to North and Central America. This clade is composed of four species that originated ~4.2 million years ago. One species from the mountains of Guatemala is sister to the other three, favoring a vicariance hypothesis of diversification. The taxonomy of the New World Cryptopone and Wadeura is revised. Taxonomic changes are as follows: Wadeura Weber is resurrected, with new combinations W. guianensis Weber, W. holmgreni (Wheeler), and W. pauli (Fernandes & Delabie); C. guatemalensis (Forel) (rev. stat.) is raised to species and includes C. obsoleta (Menozzi) (syn. nov.). The following new species are described: Cryptopone gilvagrande, C. gilvatumida, and Wadeura holmgrenita. Cryptopone hartwigi Arnold is transferred to Fisheropone Schmidt and Shattuck (n. comb.). Cryptopone mirabilis (Mackay & Mackay 2010) is a junior synonym of Centromyrmex brachycola (Roger) (syn. nov.). 

Despite recent advances in phylogenomics, the early evolution of the largest bee family, Apidae, remains uncertain, hindering efforts to understand the history of Apidae and establish a robust comparative framework. Confirming the position of Anthophorinae—a diverse, globally distributed lineage of apid bees—has been particularly problematic, with the subfamily recovered in various conflicting positions, including as sister to all other Apidae or to the cleptoparasitic Nomadinae. We aimed to resolve relationships in Apidae and Anthophorinae by combining dense taxon sampling, with rigorous phylogenomic analysis of a dataset consisting of ultraconserved elements (UCEs) acquired from multiple sources, including low-coverage genomes. Across a diverse set of analyses, including both concatenation and species tree approaches, and numerous permutations designed to account for systematic biases, Anthophorinae was consistently recovered as the sister group to all remaining Apidae, with Nomadinae sister to (Apinae, [Xylocopinae, Eucerinae]). However, several alternative support metrics (concordance factors, quartet sampling, and gene genealogy interrogation) indicate that this result should be treated with caution. Within Anthophorinae, all genera were recovered as monophyletic, following synonymization of Varthemapistra with Habrophorula. Our results demonstrate the value of dense taxon sampling in bee phylogenomics research and how implementing diverse analytical strategies is important for fully evaluating results at difficult nodes.

 

Using genetic, morphological, and geographical evidence, we investigate the species-level taxonomy and evolutionary history of the Pseudomyrmex elongatulus group, a clade of ants distributed from southwestern United States to Costa Rica. Through targeted enrichment of 2,524 UCE (ultraconserved element) loci we generate a phylogenomic data set and clarify the phylogenetic relationships and biogeographic history of these ants. The crown group is estimated to have originated ~8 Ma, in Mexico and/or northern Central America, and subsequently expanded into southern Central America and the southwestern Nearctic. The P. elongatulus group contains a mix of low- and high-elevation species, and there were apparently multiple transitions between these habitat types. We uncover three examples of one species—of restricted or marginal geographical distribution—being embedded phylogenetically in another species, rendering the latter paraphyletic. One of these cases involves an apparent workerless social parasite that occurs sympatrically with its parent species, with the latter serving as host. This suggests a sympatric origin of the parasite species within the distribution range of its host. Species boundaries are tested using three molecular delimitation approaches (SODA, bPTP, BPP) but these methods generate inflated species estimates (26–46 species), evidently because of a failure to distinguish population structure from species differences. In a formal taxonomic revision of the P. elongatulus group, based on almost 3,000 specimens from ~625 localities, we allow for geographic variation within species and we employ distinctness-in-sympatry criteria for testing hypotheses about species limits. Under these guidelines we recognize 13 species, of which nine are new: P. arcanus, sp. nov. (western Mexico); P. capillatus, sp. nov. (western Mexico); P. cognatus, sp. nov. (Chiapas, Mexico to Nicaragua); P. comitator, sp. nov. (Chiapas, Mexico); P. ereptor, sp. nov. (Veracruz, Mexico); P. exoratus, sp. nov. (southeastern Mexico, Honduras); P. fasciatus, sp. nov. (Chiapas, Mexico to Costa Rica); P. nimbus, sp. nov. (Costa Rica); and P. veracruzensis, sp. nov. (Veracruz, Mexico). Our study highlights the value of combining phylogenomic, phenotypic, and geographical data to resolve taxonomic and evolutionary questions.