Evolution in the genus Rhinella: A total evidence analysis of Neotropical true toads (Anura: Bufonidae)

PEREYRA, MARTÍN O.; BLOTTO, B. L.; BALDO, D; CHAPARRO, JUAN C.; RON, S.; ELIAS-COSTA, AGUSTIN J.; IGLESIAS, P.P.; VENEGAS, P. J.; THOME, M.T.C.; OSPINA-SARRIA, J.J.; MACIEL, NATAN; RADA, MARCO; KOLENC, F.; BORTEIRO, CLAUDIO; RIVERA-CORREA, MAURICIO; ROJAS-RUNJAIC, FERNANDO; MORAVEC, J.; DE LA RIVA, IGNACIO; WHEELER, WARD C.; CASTROVIEJO-FISHER, S.; GRANT, TARAN; HADDAD, C. F. B.; FAIVOVICH, J.

BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY

AMER MUSEUM NATURAL HISTORY

Lugar: New York; Año: 2021 vol. 447 p. 1 - 155

0003-0090

True toads of the genus Rhinella are among the most common and diverse group of Neotropicalanurans. These toads are widely distributed throughout South America, inhabiting a great diversityof environments and ecoregions. Currently, however, the genus is defined solely on the basis ofmolecular characters, and it lacks a proper diagnosis. Although some phenetic species groups havetraditionally been recognized within Rhinella, the monophyly of some of them have been rejectedin previous phylogenetic analyses, and many species remain unassigned to these poorly definedgroups. Additionally, the identity and taxonomy of several species are problematic and hinder thespecific recognition and description of undescribed taxa. In this work, we first perform phylogeneticanalyses of separate mitochondrial and nuclear datasets to test the possible occurrence of hybridizationand/or genetic introgression in the genus. The comparative analysis of both datasets revealedunidirectional mitochondrial introgressions of an unknown parental species into R. horribilis (?ghostintrogression?) and of R. dorbignyi into R. bernardoi; therefore, the mitochondrial and nuclear datasetsof these species were considered separately in subsequent analyses. We performed total-evidencephylogenetic analyses that included revised molecular (four mitochondrial and five nuclear genes)and phenotypic (90 characters) datasets for 83 nominal species of Rhinella, plus several undescribedand problematic species and multiple outgroups. Results demonstrate that Rhinella was nonmonophyleticdue to the position of R. ceratophrys, which was recovered as the sister taxon of Rhaebonasicus with strong support. Among our outgroups, the strongly supported Anaxyrus + Incilius isthe sister clade of all other species of Rhinella. Once R. ceratophrys is excluded, the genus Rhinellais monophyletic, well supported, and composed of two major clades. One of these is moderatelysupported and includes species of the former R. spinulosa Group (including R. gallardoi); the monophyleticR. granulosa, R. crucifer, and R. marina Groups; and a clade composed of the mitochondrialsequences of R. horribilis. The other major clade is strongly supported and composed of all the speciesfrom the non-monophyletic R. veraguensis and R. margaritifera Groups, the former R. acrolophaGroup, and R. sternosignata. Consistent with these results, we define eight species groups of Rhinellathat are mostly diagnosed by phenotypic synapomorphies in addition to a combination of morphologicalcharacter states. Rhinella sternosignata is the only species that remains unassigned to anygroup. We also synonymize nine species, treat three former subspecies as full species, and suggestthat 15 lineages represent putative undescribed species. Lastly, we discuss the apparently frequentoccurrence of hybridization, deep mitochondrial divergence, and ?ghost introgression?; the incompletephenotypic evidence (including putative character systems that could be used for future phylogeneticanalyses); and the validity of the known fossil record of Rhinella as a source of calibrationpoints for divergence dating analyses.