Rhinella

Pereyra, Martín O., Blotto, Boris L., Baldo, Diego, Chaparro, Juan C., Ron, Santiago R., Elias-Costa, Agustín J., Iglesias, Patricia P., Venegas, Pablo J., C. Thomé, Maria Tereza, Ospina-Sarria, Jhon Jairo, Maciel, Natan M., Rada, Marco, Kolenc, Francisco, Borteiro, Claudio, Rivera-Correa, Mauricio, Rojas-Runjaic, Fernando J. M., Moravec, Jiří, De La Riva, Ignacio, Wheeler, Ward C., Castroviejo-Fisher, Santiago, Grant, Taran, Haddad, Célio F. B. & Faivovich, Julián, 2021, Evolution In The Genus Rhinella: A Total Evidence Phylogenetic Analysis Of Neotropical True Toads (Anura: Bufonidae), Bulletin of the American Museum of Natural History 2021 (447), pp. 1-157 : 7-8

SYSTEMATICS OF RHINELLA

For decades, all South American true toads were part of the formerly large and poorly defined genus Bufo , which included a heterogeneous group of toads distributed throughout Africa, America, and Eurasia (e.g., Blair, 1972; Graybeal, 1997). Frost et al. (2006) partitioned this polyphyletic genus into monophyletic units mostly on the basis of the results of their phylogenetic analysis but also on the results of previous studies (e.g., Graybeal, 1997; Pauly et al., 2004). Frost et al. (2006) resurrected Rhinella for the species of the former Bufo margaritifer Group, which they recovered as distantly related to the other species of South American true toads included in their analysis, including Chaunus and Rhaebo (both also resurrected by Frost et al., 2006). Frost et al. (2006) noted that Bufo margaritifer was nested within Chaunus in a previous phylogenetic study (Pauly et al., 2004), a finding that was subsequently supported by Pramuk (2006) and Chaparro et al. (2007). Therefore, Rhinella was later redefined to include the species of Chaunus and Rhamphophryne as well ( Chaparro et al., 2007).

The species groups of the former Bufo now referred to Rhinella were all recognized primarily on the basis of osteological characters and external morphology that were interpreted without quantitative phylogenetic analyses (Tihen, 1962; Cei, 1972a; R.F. Martin, 1972a, 1972b; Duellman and Schulte, 1992), including the R. crucifer , R. granulosa , R. margaritifera , R. marina , R. spinulosa , and R. veraguensis Groups. Pramuk (2006) studied the phylogenetic relationships of these toads on the basis of a combined analysis of morphological (mostly osteological) and molecular evidence. She rejected the monophyly of some of these species groups (e.g., the R. veraguensis Group is polyphyletic with respect to R. ocellata , the R. margaritifera Group, and Rhamphophryne ), but did not modify their composition or diagnosis.

The subsequent increase in the knowledge of relations within Rhinella was limited to the addition of available sequences of some species in extensive phylogenetic analyses of Bufonidae or Anura (e.g., van Bocxlaer et al., 2010; Pyron and Wiens, 2011; Pyron, 2014; Jetz and Pyron, 2018). Figure 1 summarizes the main results of the more inclusive analyses of Rhinella .

For well over a decade, the systematics of Rhinella as a whole has languished, although several efforts focusing on the relationships and taxonomy of parts of the genus have been undertaken. These include phylogenetic analyses of presumptively monophyletic species groups (i.e., the R. crucifer , R. granulosa , and R. marina Groups ; Maciel et al., 2006, 2010; Thomé et al., 2010, 2012; Vallinoto et al., 2010; Pereyra et al., 2016a) or fractions of the diversity of certain groups (i.e., the R. festae and R. margaritifera Groups ; Fouquet et al., 2007a; Moravec et al., 2014; Santos et al., 2015; Cusi et al., 2017; Avila et al., 2018). Most recent studies on Rhinella aimed primarily to resolve species-level taxonomic problems (e.g., Fouquet et al., 2007a; Narvaes and Rodrigues, 2009; Jansen et al., 2011; Grant and Bolívar-G., 2014; Moravec et al., 2014; Cusi et al., 2017). Consequently, more than a decade after Pramuk’s (2006) revision, species groups remain poorly defined, several species cannot be assigned to any of them, and few additional phenotypic synapomorphies have been proposed for Rhinella or its internal clades ( Hoogmoed, 1986; 1990; La Marca and Mijares- Urrutia, 1996; Pramuk, 2006; Chaparro et al., 2007; Padial et al., 2009; Blotto et al., 2014; Grant and Bolívar-G., 2014; Pereyra et al., 2016a).

Natural hybridization is common in several groups of Bufonidae , including many species of Rhinella ( Blair, 1972; Feder, 1979; Haddad et al., 1990; Masta et al., 2002; Azevedo et al., 2003; Green and Parent, 2003; Yamazaki et al., 2008; Fontenot et al., 2011; Guerra et al., 2011), and mitochondrial and nuclear introgression have been corroborated in some of these clades (e.g. Green and Parent, 2003; Yamazaki et al., 2008; Fontenot et al., 2011; Dufresnes et al., 2019). Pereyra et al. (2016a) demonstrated the occurrence of hybridization events in the R. granulosa Group and unidirectional mitochondrial introgression of R. dorbignyi into R. bernardoi. A similar situation might exist between R. marina and R. diptycha , although the evidence is not conclusive (Sequeira et al., 2011; Vallinoto et al., 2017). The impact of these phenomena on the inference of phylogenetic relationships ( Hennig, 1966; McDade, 1992; Posada and Crandall, 2002) could be mitigated, at least partially, if detected. A detailed evaluation of the discordance between mitochondrial and nuclear genomes together with a critical taxonomic evaluation provide an effective way to detect hybridization/introgression (Pereyra et al., 2016a).

In this paper, we present a densely sampled phylogenetic analysis of Rhinella , including 83 of its 92 species, using molecular (four mitochondrial and five nuclear genes) and phenotypic characters (90 characters from multiple character systems). The goals of this study are to (1) perform a stringent test of the monophyly of Rhinella as well as similar tests on all its species groups, (2) identify phenotypic synapomorphies to diagnose the species groups of Rhinella , and (3) to evaluate the taxonomic status of several taxa.

Figures

FIG. 1. Summarized relationships of Rhinella according to the main published phylogenetic hypotheses of the group. Only the topological sections corresponding to Rhinella, and putative most related outgroups (i.e., Anaxyrus and Incilius) are shown. The number of species sampled within each clade is reported in parentheses. (A) Pauly et al. (2004: fig. 2). (B) Frost et al. (2006: fig. 50). (C) Pramuk (2006: fig. 4). (D) Chaparro et al. (2007: fig. 9). (E) van Bocxlaer et al. (2010: fig. S1). (F) Pyron and Wiens (2011: fig. 2). (G) Pyron (2014: suppl. information “amph_shl.tre”). (H) Pereyra et al. (2016a: fig. 3 and appendix S12). (I) Jetz and Pyron (2018: suppl. information “amph_shl_new.tre”).