Research Overview

Research in the Rabeling Lab integrates organismal evolutionary biology and ecology to study biodiversity and elucidate the evolutionary patterns and processes underlying biological speciation. Discovering and describing new species, as well as understanding how new species originate and how biodiversity is maintained in our ecosystems is important for developing strategies against the global biodiversity crisis. Our studies focus on ants, because their high diversity, ecological dominance, complex social behaviors, and diverse symbiotic interactions make them ideal study systems for exploring long-standing questions in ecology, evolutionary biology, and biodiversity research.

Diversity & Evolution of Ant Social Parasites

 

Studying the repeatedly evolved behavioral and life history transitions from eusociality to social parasitism allow for understanding the rare conditions under which changes in behavior and social organization lead to speciation. Our research program aims at unraveling the complex evolutionary history of ant social parasites and their hosts, and seeks to understand the influence that convergently evolved behavioral changes have on the speciation patterns and mechanisms generating social parasite diversity. Ant social parasites rely on the social organization of their ant hosts for survival and reproduction, they are speciose with more than 400 known species, and they are phylogenetically diverse with at least 91 convergent origins.Therefore, ant social parasites represent a set of natural experiments that allow us to study the ecological, behavioral, and genetic mechanisms, by which a switch from eusocial to parasitic behavior leads to reproductive isolation in direct sympatry.The goals of our ant social parasite research program are to (i) reconstruct the speciation patterns and the evolutionary history of social parasite diversification, (ii) unearth the global biodiversity of social parasite by using an integrative approach to biodiversity discovery and social parasite taxonomy, effectively delimiting species and revising ant social parasites across the ant tree of life, and (iii) decipher the genetic mechanisms underlying social parasite speciation and evolution, identifying the genomic modifications that are consistently associated with social parasite evolution. In summary, we use an integrative approach to organismal evolutionary biology, exploring how socially parasitic ant lineages originated repeatedly and convergently from their eusocial ancestors.

 

Selection of ant social parasite evolution papers:

  • Dahan RA, Rabeling C. 2022. Multi-queen breeding is associated with the origin of inquiline social parasitism in ants. Scientific Reports 12:14680
  • Gray KW, Rabeling C. 2023. Global biogeography of ant social parasites: exploring patterns and mechanisms of an inverse latitudinal diversity gradient. Journal of Biogeography 50: 316–329 
  • Mera-Rodríguez LD, Jourdan H, Ward PS, Shattuck SO, Cover SP, Wilson EO, Rabeling C. 2023. Biogeography and evolution of social parasitism in Australian Myrmecia bulldog ants revealed by phylogenomics. Molecular Phylogenetics and Evolution 186: 107825

Biodiversity & Island Biogeography of South Pacific Ants

 

With their variations in size, age, biological complexity, and ecology, islands are replicates of natural experiments and truly original insights into evolutionary biology and ecology have resulted from studies of island biota. To study the island biogeography and ant biodiversity of Melanesia, we embarked on a biodiversity exploration project, surveying the ant fauna of the South Pacific island archipelago Vanuatu. The Vanuatuan ant fauna was never surveyed systematically, and not surprisingly, we roughly tripled the number of ant species known from Vanuatu to currently 130 species, several of which are endemic to Vanuatu and new to science. Our goals of this island biogeography research are to write a taxonomic monograph about the Ants of Vanuatu, and use the specimen data to test for rapid speciation events and endemic evolutionary radiations, effectively revisiting Wilson's early formulation of the 'taxon cycle', which is an ecological model addressing speciation on islands. Importantly, the Anthropocene is characterized by rapid biodiversity loss due to man-made habitat destruction and pollution. The Theory of Island Biogeography provides the intellectual framework for conservation biology because species cling to remnants of natural habitat, which are insular by definition, and experience disturbances and extinction events. Hence, our ongoing island biogeography research is not only expected to teach us about the biodiversity and biogeography of Vanuatuan ants but also provide lessons for conservation biology.

 

Selection of island biogeography papers:

  • Sarnat EM, Rabeling C, Economo EP, Wilson EO. 2014. First record of a species from the Pheidole flavens -complex (Hymenoptera: Formicidae) from the southwestern Pacific. BioInvasions Records 3: 301–307 
  • Clouse RM, Janda M, Blanchard B, Sharma P, Hoffman BD, Andersen AN, Czekanski-Moir JE, Krushelnycky P, Rabeling C, Wilson EO, Economo EP, Saranat EM, Wheeler WC. 2014. Molecular phylogeny of a widespread ant group reveals waves of dispersal and colonization into and out of the Pacific. Cladistics 31: 424–437
  • Economo EP, Sarnat EM, Janda M, Clouse R, Klimov P, Fischer G, Blanchard BD, Ramirez L, Andersen AN, Berman M, Guénard B, Rabeling C, Wilson EO, Knowles LL. 2015. Breaking out of biogeographic modules: range expansion and taxon cycles in Old World Pheidole . Journal of Biogeography 42: 2253–2460 
  • Matos-Maraví P, Clouse RM, Sarnat EM, Economo EP, LaPolla JS, Borovanska M, Rabeling C, Czekanski-Moir J, Latumahina F, Wilson EO, Janda M. 2018. An ant genus-group (Prenolepis ) illuminates the biogeography and drivers of insect diversification in the Indo-Pacific. Molecular Phylogenetics and Evolution . 123:16-25 

Phylogenomics & Early Ant Evolution

 

To infer the evolutionary history of ants and test competing hypotheses about their diversification, ecology, and life history evolution, a robust phylogenetic framework is indispensable. Our research makes extensive use of phylogenetic/phylogenenomic techniques to infer the evolution of parasitic and mutualistic behaviors in social insects, to understand how mutualism and parasitism contribute to the speciation process, as well as to integrate taxonomy with phylogenetic classification. In 2008, we described a unique ant species that we discovered in the Brazilian Amazon as Martialis heureka. To accommodate this species' unique mosaic of plesiomorphic and derived morphological characters, we erected a new ant subfamily, the Martialinae. Using a 3-gene phylogeny at the time, we inferred Martialis as the sister lineage to all extant ants. Our subsequent phylogenetic analyses utilized significantly larger molecular datasets, revealing a sister taxon relationship between the Martialinae and the Leptanillinae, both forming the sister group to all extant ants. A recent reconstruction of the ant tree of life using whole genome sequences confirmed the phylogenetic placement of Martialis as the sister group to the Leptanillinae. Considering that both Martialis and the Leptanillinae are subterraneous predators and that Martialis is of Neotropical origin whereas the Leptanillinae are distributed throughout the Old World, it remains interesting to investigate the biology and biogeography of these ancient ant lineages. Generally speaking, the robust phylogenies we can generate today with genomic data serve as essential research tools for testing competing hypotheses about the biology and evolution of ants (or any other group of organisms).

 

Selection of ant evolution papers:

Ant-Fungus Co-evolution in Fungus-Growing Ants

 

Symbioses between distantly related species are ubiquitous across the tree of life (e.g., mitochondria in eukaryotic cells or plants and mycorrhizal fungi) and their co-evolutionary interactions significantly shape the evolution of biological complexity. In the past decades, the symbiosis between fungus-growing or "attine" ants, their mutualistic and parasitic fungi, as well as associated microbes developed into a model system for exploring questions about co-evolutionary dynamics. The fungus-growing ants are a monophyletic group of approximately 250 exclusively New World ant species that started cultivating fungi about 60 million years ago. In collaboration with the Mueller Lab at the University of Texas at Austin and the Schultz Lab at the Smithsonian Institution, we have been conducting taxonomic, phylogenetic, evolutionary biology, and natural history studies, in which we described new species and genera of fungus-growing ants, inferred the co-evolution between attine ants and their mutualistic fungi, as well as studied fungus-growing ant biology in the field. Currently, our research activities focus on the evolution and diversity of leaf-cutting ants and their obligate ant social parasites.

 

Selection of fungus-growing ant papers:

  • Rabeling C, Cover SP, Mueller UG, Johnson RA. 2007. A review of the North American species of the fungus-gardening ant genus Trachymyrmex (Hymenoptera: Formicidae). Zootaxa 1664: 1–54 
  • Sosa-Calvo J, Schultz TR, Brandão CRF, Klingenberg C, Feitosa RM, Rabeling C, Bacci M, Lopes CT, Vasconcelos HL. 2013.  Cyatta abscondita : Taxonomy, evolution, and natural history of a new fungus-farming ant genus from Brazil. PLoS ONE 8(11): e80498 
  • Mueller UG, Ishak HD, Brushi SM, Herman JJ, Smith CC, Solomon SE, Mikheyev AS, Rabeling C, Scott JJ, Cooper M, Rodriguez A, Ortiz A, Brandão CRF, Lattke JE, Pagnocca FC, Rehner SA, Schultz TR , Vasconcelos HL, Adams RMM, Bollazzi M, Clark RM, Himler AG, LaPolla JS, Leal IR, Johnson RA, Roces F, Sosa-Calvo J, Wirth R, Bacci Jr M. 2017. Biogeography of mutualistic fungi cultivated by leafcutter ants . Molecular Ecology 26: 6921–6937 
  • Sosa-Calvo J, Schultz TR, Ješovnik A, Dahan RA, Rabeling C. 2018. Evolution, systematics, and natural history of a new genus of cryptobiotic fungus-growing ants. Systematic Entomology 43: 549–567 
  • Li H, Sosa-Calvo J, Horn H, Pupo MT, Clardy J, Rabeling C, Schultz TR, Currie CR. 2018. Convergent evolution of complex structures for ant-bacterial defensive symbiosis in fungus-farming ants. Proceedings of the National Academy of Sciences of the United States of America 115: 10720–10725 
  • Solomon SE, Rabeling C, Sosa-Calvo J, Lopes CT, Mueller UG, Vasconcelos HL, Bacci M, Schultz TR. 2019. Molecular phylogenies of Trachymyrmex ants and their fungal cultivars provide insights into the co-evolutionary history of "higher" ant agriculture. Systematic Entomology 44: 939–956 
  • Barrera C, Sosa-Calvo J, Schultz TR, Rabeling C, Bacci M. 2022. Phylogenomic reconstruction reveals new insights into the evolution and phylogeography of Atta leaf-cutting ants (Hymenoptera: Formicidae). Systematic Entomology 47: 13–35 
  • Schultz TR, Sosa-Calvo J#, Kweskin MP, Lloyd MW, Dentinger B, Kooij PW, Vellinga EC, Rehner SA, Rodrigues A, Montoya QV, Fernández-Marín H, Ješovnik A, Niskanen T, Liimatainen K, Leal-Dutra CA, Solomon SE, Gerardo NM, Currie CR, Bacci Jr. M, Vasconcelos HL, Rabeling C, Faircloth BC, Doyle VP. The coevolution of fungus-ant agriculture. Science 386: 105–109

Evolutionary Ecology of Asexual Reproduction in Ants

 

Evolutionary theory predicts that organisms relying on asexual reproduction risk rapid extinction due to the lack of genetic diversity. In contrast, sexually reproducing organisms benefit from the continuous creation of genetic variation by recombination, which allows efficient purging of deleterious mutations from the genome and rapid evolutionary responses to changing selective pressures from the biotic and abiotic environment. At the same time generating genetic novelty is costly. Having two sexes, expending energy during courtship, and falling victim to sexually transmitted diseases are just a few of the detriments associated with sexual reproduction. To explore the benefits and costs of asexual vs. sexual reproduction, we explore the evolutionary ecology of the parthenogenetic fungus-growing ant  Mycocepurus smithii. Our current understanding is that the asexual M. smithii is a single, monophyletic species, consisting of a mosaic of asexual and sexual populations where rare sexual populations repeatedly give rise to geographically widespread, strictly clonal lineages that are able to rapidly exploit novel ecological niches across Central and South America. Cytogenetic evidence suggests that the lack of genetic recombination causes a decay of the homologous chromosome pair structure in asexual lineages. Despite these first insights, much remains to learn about the evolutionary ecology of this unique ant species.

 

Selection of ant asexuality papers:

  • Rabeling C, Lino Neto J, Cappellari SC, Santos IA, Mueller UG, Bacci M. 2009. Thelytokous parthenogenesis in the fungus-gardening ant Mycocepurus smithii (Hymenoptera: Formicidae). PLoS ONE 4(8): e6781
  • Rabeling C, Gonzales O*, Schultz TR, Bacci M, Garcia MVB, Verhaagh M, Ishak H*, Mueller UG. 2011. Cryptic sexual populations account for genetic diversity and ecological success in a widely distributed, parthenogenetic fungus-growing ant. Proceedings of the National Academy of Sciences of the United States of America 108: 12366–12371
  • Rabeling C & Kronauer DJC. 2013. Thelytokous parthenogenesis in eusocial Hymenoptera. Annual Review of Entomology 58: 273–292
  • Masiulionis VE, Rabeling C, De Fine Licht HH, Schultz TR, Bacci Jr. M, Santos Bezerra CM, Pagnocca FC. 2014. A Brazilian population of the asexual fungus-growing ant Mycocepurus smithii (Formicidae, Myrmicinae, Attini) cultivates fungal symbionts with gongylidia-like structures. PLoS ONE 9(8): e103800 
  • Barros LAC, Rabeling C, Teixeira GA, Mariano CSF, Delabie JHC, de Aguiar HJAC. 2022. Decay of homologous chromosome pairs and discovery of males in the Lytokous fungus-growing ant Mycocepurus smithii . Scientific Reports 12: 4860

 

 

Ant photo credit: Alex Wild/alexanderwild.com