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Phylogenetic Analysis of the Subfamily Hylodinae (Anura, Leptodactylidae) Based on Morphological Characters

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Phylogenetic Analysis of the Subfamily Hylodinae (Anura, Leptodactylidae) Based on Morphological Characters Amphibia-Reptilia 26 (2005): 139-147 Phylogenetic analysis of the subfamily Hylodinae (Anura, Leptodactylidae) based on morphological characters Paulo A.S. Nuin1, Francisca C. do Val2 Abstract. The systematics and phylogenetic relationships of the family Leptodactylidae are controversial as is the intrafamilial phylogeny of the leptodactylids. Here we analyze the relationships of the leptodactylid subfamily Hylodinae. This subfamily has been considered to be monophyletic and composed of three genera, Hylodes, Crossodactylus and Megaelosia. In the present study 49 characters were used, based on different studies on Leptodactylidae phylogeny. Maximum parsimony methods with unweighted and successively weighted characters were used to estimate the phylogeny of the Hylodinae. Upon analysis, the data provided further evidence of the monophyletic status of the three genera, with Megaelosia being the basal genus and the other two genera being sister taxa. The analysis with successive weighting results in a more resolved topology of the species subgroups of the genus Hylodes and separates this genus from Crossodactylus and confirms that the hylodines are monophyletic. Introduction ered ancestral to the Dendrobatidae, but this arrangement was later refuted by Ford (1993). According to Lynch (1971), the subfamily Hy- Lynch (1971), in his extensive work on lep- lodinae Günther 1858 (Anura, Leptodactyli- todactylids, considered Hylodes, Crossodacty- dae) is composed of three genera of small and lus and Megaelosia to belong to a separate medium-sized [3-15 cm Snout-Vent Length, monophyletic subfamily, based mainly on re- SVL] Neotropical frogs: Hylodes, Crossodacty- sults obtained from osteological and myological lus and Megaelosia. At present these genera characters. In the most recent re-classification contain 19, 10 and 6 species, respectively (Frost, Frost (2002), based on data from Laurent 2002; Pombal et al., 2003). Frogs in all three (1986), included these genera in the subfamily genera are morphologically homogeneous, with Cycloramphinae, which includes six other ge- Megaelosia being larger and having a distinct nera. cranial morphology. The 35 described species Hylodes Fitzinger 1826 includes 20 de- of this group are diurnal, commonly associated scribed species that are mainly distinguished with mountain streams, and their distribution by their morphological characteristics. They is restricted primarily to the Brazilian Atlantic can be classified into four different species Rain Forest. The one exception is Crossodacty- groups: lateristrigatus, mertensi, glaber and na- lus schmidti which inhabits the forests of the sus (Heyer, 1982; Heyer and Cocroft, 1986; Northeast of Argentina. Frost, 1985; Duellman, 1993; Glaw et al., Originally, Noble (1922, 1931) considered 1998; Frost, 2002). Due to their morpholo- these three genera as bufonids, a conclusion that gical similarity, there are still many taxo- was changed later with the inclusion of these nomic issues to be resolved with regards to species in the Leptodactylidae (Davis, 1936). their intrageneric classification. Two groups, Due to a large number of morphological sim- mertensi and glaber, include single ilarities, the subfamily Hylodinae was consid- species which are now thought to be extinct, as collection efforts have been unsuccessful for 1 - Department of Biology, McMaster University, 1280 over 20 years (Heyer, pers. comm.). The species Main St. W. Hamilton, ON Canada L8S 4K1 included in the lateristrigatus group vary in e-mail: [email protected] 2 - Museu de Zoologia, Universidade de São Paulo, Av. body size between small to medium SVL, have Nazareth, 481, Sao Paulo SP Brazil 04263-000 a slender body, and have a distinct white dor- © Koninklijke Brill NV, Leiden, 2005. Also available online - www.brill.nl 140 P.A.S. Nuin, F.C. do Val solateral stripe. Species from the nasus group have used the genera, not the species as units are slightly larger and lack the lateral stripes. of analysis. The purposes of this study are to All members of this genus have a distribution re-evaluate the relationships among the genera ranging from the North-East to the South of based on more intensive species and character Brazil. sampling and to determine whether these three The frogs of the genus Crossodactylus have genera comprise a monophyletic clade based on a distribution that is similar to that of the genus this expanded data set. Hylodes, with one species in the North-East of Argentina (Crossodactylus schmidti, Misiones Province). In general these frogs are smaller Material and methods than Hylodes species. These species can be di- A total of 13 hylodine and 11 other leptodactylid species vided into three different groups: gaudichaudii, were selected to be part of the analysis (table 1). Despite trachystomus and schmidti (Caramaschi and scarce museum collections and difficulties in collecting in- Sazima, 1985) based mainly on differences in dividuals of Hylodes, Crossodactylus and Megaelosia,we snout and canthus rostralis morphology. Ac- attempted to select species representing the diversity found in each of the Hylodinae genera. In Hylodes, species rep- cording to Lynch (1971), Crossodactylus is also resenting each of the subgroups were obtained, except for characterised by several primitive characters the mertensi and glaber groups, which appear to be extinct. (larval morphology, secondary sexual charac- Crossodactylus species from distant geographical regions ters) and some derived ones (loss of quadrato- and two distinct subgroups were also selected. A single Megaelosia (M. goeldii) was included because of difficul- jugal). ties in obtaining specimens. The outgroup was composed of In number of species, Megaelosia is the species from the three other subfamilies of Leptodactylidae, smallest genus in the group, composed of only including representatives from distinct geographic regions. 6 large (10-15 cm SVL) frog species endemic From the 49 characters analyzed (Appendix), 35 (1-35) were defined in the study of Heyer (1975). Heyer used ge- to the Atlantic Rain Forest of the states of nera as the Operational Taxonomic Units (OTU) whereas São Paulo, Minas Gerais, Rio de Janeiro and we use species as the OTUs as indicated previously. Char- Espírito Santo, South-Eastern Brazil (Giaretta acter numbers 36 to 40 were defined in a study of Physalae- et al., 1993; Pombal et al., 2003). Megaelosia mus osteology by Lobo (1994). The other nine characters (41-49) were adapted from Heyer (1973) in his study of the has been considered to be the most primitive genus Leptodactylus (L. marmoratus group). genus of the subfamily Hylodinae, as it has dis- The analysis of external characters was performed, when tinct cranial structures, increased maxilla and possible, with 10 specimens of each gender. Osteology and quadratojugal and occipital condyles (Lynch, myology were assessed from one specimen of each species. After the myological data were taken, the specimens were 1971). The squamosal architecture is distinct cleared and stained (Taylor and Van Dyke, 1985). from Hylodes and Crossodactylus, but based on We carried out Maximum Parsimony (MP) analyses us- external morphology of adults, Megaelosia has ing PAUP* (Swofford, 2002) and performing branch and been assigned to the Hylodinae. bound searches and tree bissection reconnection branch- swapping heuristic searches. All characters were considered All previous studies treating relationships of ordered according to Wilkinson (1992) and Campbell and the genera Crossodactylus, Hylodes, and Mega- Frost (1993). Two analyses were carried out, one with un- elosia have been based on very limited taxon weighted and one with successive weighting (Farris, 1969) sampling within these genera. For example, with weights being applied according to the Retention Index Lynch (1971) examined 3 species of Crosso- (RI) until achieving stability in the number of steps. When more than one tree resulted from the analysis, a strict con- dactylus, 5 species of Hylodes, and 1 species of sensus tree was calculated. Megaelosia, while Heyer (1975) examined 1, 2, Branch stability was accessed by the Bremer index (Bre- and 1 species respectively of these genera (of mer, 1988; Källersjö et al., 1992; Bremer, 1994) calculated the same species Lynch examined). There are no using AutoDecay PPC version 4.01 (Eriksson, 2002). Boot- strap (Felsenstein, 1985) and jackknife (only in the un- rigorous analyses of interspecific relationships weighted analysis) (Farris et al., 1996) analyses were also for these genera. All previous rigorous analyses performed, each with 1000 pseudoreplications. Phylogeny of Hylodinae 141 Table 1. List of the leptodactylid species analyzed to obtain phylogenetic relationships. Subfamily Genera species subgroup Hylodinae Hylodes lateristrigatus lateristrigatus asper nasus phyllodes lateristrigatus ornatus lateristrigatus sazimai lateristrigatus nasus nasus meridionalis nasus perplicatus nasus dactylocinus nasus Crossodactylus caramaschii gaudichaudii dantei gaudichaudii schmidti schmidti Megaelosia goeldii – Leptodactylinae Leptodactylus knudseni – Leptodactylus ocellatus – Physalaemus cuvieri – Telmatobiinae Alsodes gargola – Eupsophus calcaratus – Thoropa miliaris – Cycloramphus boraceiensis – Cycloramphus semipalmatus – Eleutherodactylus fenestratus – Ceratophrynae Proceratophrys boiei – Odontophrynus americanus – Results the two other Hylodinae genera. Bootstrap and Bremer values obtained for both methods were The unweighted phylogenetic analysis resulted similar.
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