Global domination by crazy ants: phylogenomics reveals biogeographical history and invasive species relationships in the genus Nylanderia (Hymenoptera: Formicidae)

Abstract

Nylanderia (Emery) is one of the world's most diverse ant genera, with 123 described species worldwide and hundreds more undescribed. Fifteen globetrotting or invasive species have widespread distributions and are often encountered outside their native ranges. A molecular approach to understanding the evolutionary history and to revision of Nylanderia taxonomy is needed because historical efforts based on morphology have proven insufficient to define major lineages and delimit species boundaries, especially where adventive species are concerned. To address these problems, we generated the first genus‐wide genomic dataset of Nylanderia using ultraconserved elements (UCEs) to resolve the phylogeny of major lineages, determine the age and origin of the genus, and describe global biogeographical patterns. Sampling from seven biogeographical regions revealed a Southeast Asian origin of Nylanderia in the mid‐Eocene and four distinct biogeographical clades in the Nearctic, the Neotropics, the Afrotropics/Malagasy region, and Australasia. The Nearctic and Neotropical clades are distantly related, indicating two separate dispersal events to the Americas between the late Oligocene and early Miocene. We also addressed the problem of misidentification that has characterized species‐level taxonomy in Nylanderia as a result of limited morphological variation in the worker caste by evaluating the integrity of species boundaries in six of the most widespread Nylanderia species. We sampled across ranges of species in the N. bourbonica complex (N. bourbonica (Forel) + N. vaga (Forel)), the N. fulva complex (N. fulva (Mayr) + N. pubens (Forel)), and the N. guatemalensis complex (N. guatemalensis (Forel) + N. steinheili (Forel)) to clarify their phylogenetic placement. Deep splits within these complexes suggest that some species names – specifically N. bourbonica and N. guatemalensis – each are applied to multiple cryptic species. In exhaustively sampling Nylanderia diversity in the West Indies, a ‘hot spot’ for invasive taxa, we found five adventive species among 22 in the region; many remain morphologically indistinguishable from one another, despite being distantly related. We stress that overcoming the taxonomic impediment through the use of molecular phylogeny and revisionary study is essential for conservation and invasive species management.

Wolbachia Infection in Native Populations of the Invasive Tawny Crazy Ant Nylanderia fulva

“…In addition, N. pubens was placed within the boundaries of what we considered the species N. fulva , and thus supports its position as a sibling species. This is in line with a recent work suggesting that N. fulva and N. pubens form a species complex ( 29 ). These two species have been commonly mistaken due to the identical aspect of their workers, but are distinguishable inspecting male genital characters ( 18 ).…”

Phylogenomic reconstruction reveals new insights into the evolution and biogeography of Atta leaf‐cutting ants (Hymenoptera: Formicidae)

“…Our study adds to a growing body of phylogenetic research that utilizes UCEs to infer comprehensive, well-resolved, and statistically well-supported phylogenies in order to study insect evolution, as well as to test evolutionary and biogeographic hypotheses (Faircloth et al, , 2015Blaimer et al, 2016a;Branstetter et al, 2017cBranstetter et al, , 2021. Lending support to the conclusions of multiple prior studies, our results indicate that UCEs are extremely effective for reconstructing divergences in higher-attine and other groups of ants at a wide range of levels, from ancient (>30 Ma) to very recent, including the delimitation of species and populations, even in very recent, short-branched evolutionary radiations (Blaimer et al, 2016b;Ješovnik et al, 2017;Branstetter et al, 2017a;Borowiec et al, 2020;Prebus, 2020;Williams et al, 2020;van Elst et al, 2021;Rabeling et al in prep. ).…”

Phylogeny, evolution, and classification of the ant genus Lasius, the tribe Lasiini and the subfamily Formicinae (Hymenoptera: Formicidae)

“…pygmaea was assigned during node calibration. While Blaimer et al (2015) and our study do not include any Nylanderia fossils, Matos-Maraví et al ( 2018) and Williams et al (2020) included †N. pygmaea, with this species assigned to the stem of Nylanderia in the former and to the crown of Nylanderia in the latter (Jason Williams & John LaPolla pers.…”

“…Notably, the crown lineages of the Lasius genus group have failed to invade tropical zones, whereas at least two invasions of the temperate zone have occurred in the Prenolepis genus group, once each for the imparis clade of Prenolepis and the vividula clade of Nylanderia. A third invasion is implied byMatos-Maraví et al (2018) andWilliams et al (2020) for…”