PSEUDOXENODONTIDAE

Grazziotin, Hussam Zaher 1 Felipe Gobbi, Cadle, John E., Murphy, Robert W., Moura-Leite, Julio Cesar de & Bonatto, Sandro L., 2009, Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: a revised classification and descriptions of new taxa, Papéis Avulsos de Zoologia 49 (11), pp. 115-153 : 139-141

FAMILY PSEUDOXENODONTIDAE

McDowell, 1987 (terminal taxon: Pseudoxenodon karlschmidti )

Pseudoxenodontinae McDowell, 1987: 38 .

Type-genus: Pseudoxenodon Boulenger, 1890 . Diagnosis: Hemipenis deeply bilobed, with each lobe separately calyculate on the distal half and nude on the medial half; fringes of large papillae separating the nude region from the calyculate area (Zaher, 1999).

Content: Plagiopholis Boulenger, 1893 ; Pseudoxenodon Boulenger, 1890 .

Comments: He et al. (2009) demonstrated that Plagiopholis is indeed closely related to Pseudoxenodon .

FAMILY NATRICIDAE Bonaparte, 1838 (Clade 24)

Natricina Bonaparte, 1838: 392.

Type-genus: Natrix Laurenti, 1768 .

Diagnosis: (89%, 12). Sulcus spermaticus single and highly centripetal, forming a nude region on the medial surfaces of the hemipenial lobes; hemipenial calyces absent (evolutionary loss).

Content: Adelophis Dugès (in Cope), 1879; Afronatrix Rossman & Eberle, 1977 ; Amphiesma Duméril, Bibron & Duméril, 1854 ; Amphiesmoides Malnate, 1961 ; Anoplohydrus Werner, 1909 ; Aspidura Wagler, 1830 ; Atretium Cope, 1861 ; Balanophis Smith, 1938 ; Clonophis Cope, 1888 ; Hologerrhum Günther, 1858 ; Hydrablabes Boulenger, 1891 ; Hydraethiops Günther, 1872 ; Limnophis Günther, 1865 ; Lycognathophis Boulenger, 1893 ; Macropisthodon Boulenger, 1893 ; Natriciteres Loveridge, 1953 ; Natrix Laurenti, 1768 ; Nerodia Baird (in Baird & Girard), 1853; Opisthotropis Günther, 1872 ; Parahelicops Bourret, 1934 ; Pararhabdophis Bourret, 1934 ; Regina Baird (in Baird & Girard), 1853; Rhabdophis Fitzinger, 1843 ; Seminatrix Cope, 1895 ; Sinonatrix Rossman & Eberle, 1977 ; Storeria Girard (in Baird & Girard), 1853; Thamnophis Fitzinger, 1843 ; Tropidoclonion Cope, 1860 ; Tropidonophis Jan, 1863 ; Virginia Girard (in Baird & Girard), 1853; Xenochrophis Günther, 1864 .

Comments: Among Natricidae , the New World natricids are a monophyletic tribe (Thamnophiini) supported by molecular and morphological evidence ( Rossman & Eberle 1977; Alfaro & Arnold 2001; De Queiroz et al. 2002). Relationships among African and Eurasian species are largely unresolved. See Comments under Colubridae concerning differences between the simple sulci spermatici of natricids and colubrids.

FAMILY DIPSADIDAE Bonaparte, 1838 (Clade 25)

Diagnosis: (*, 9). A row of enlarged lateral spines on each side of the hemipenis; hemipenial lobes with distinct differentially ornamented regions (a sulcate capitulum and an asulcate nude or weakly calyculate region) (Zaher, 1999).

Content: Dipsadinae Bonaparte 1838 , Carphophiinae new subfamily, and Xenodontinae Bonaparte 1845.

Comments: The diagnosis we give here for Dipsadidae includes those synapomorphies previously considered for the more restricted group Xenodontinae (sensu Zaher, 1999). We present them here for Dipsadidae because the North American Farancia and Heterodon also have these characters. Thus, these characters could have separately evolved in Farancia and Heterodon , and South American xenodontines (with subsequent loss in Carphophis , Contia , and Diadophis ); or, the interpretation we adopt here, the characters could be synapomorphic at the level of Dipsadidae , with subsequent transformations (losses) in the clade including Carphophis , Contia , and Diadophis on one hand, and in Dipsadinae on the other. This question must be resolved with further research. In any case, we note that there is evidence from the present study and from the immunological comparisons of Cadle (1984a,b,c) for three major clades within the Dipsadidae as we conceive it, namely a North American clade, a Dipsadinae clade, and a Xenodontinae clade (see also Pinou et al., 2004). However, Pinou et al. (2004) found the North American xenodontines (their North American relicts) paraphyletic with respect to dipsadines, xenodontines, and natricids. The monophyly of the North American xendontines was also unstable in the present analysis, with a low bootstrap support on Clades 23, 25, and 30 due to the variable positions of Heterodon and Farancia with respect to these nodes in suboptimal trees. Thus, further revisions on that issue may be warranted. On the other hand, Carphophis , Contia , and Diadophis form a well-supported clade (Clade 29; 88%, 4) corroborated by putative hemipenial synapomorphies. Those synapomorphies also support the clade Dipsadinae (Clade 31; 74%, 7) and are here viewed as having evolved homoplastically in these two groups. The optimization of these characters on the tree depends on a better understanding of the position of Heterodon and Farancia that are here included in Dipsadidae incertae sedis.

The genus Xenopholis Peters, 1869 , not included in the present analysis, has been recently associated with the Xenodermatidae by Dowling & Pinou (2003). However, its dipsadid hemipenial morphology, the presence of a well-developed septomaxillary-frontal articulation, and previous immunological studies do not support the latter hypothesis ( Cadle, 1984a), suggesting dipsadid affinities instead (see also discussion above in Xenodermatidae ). Since the position of Xenopholis within the Dipsadidae is still unknown, we opted to include it in the family as incertae sedis, but we have no reservations at all about its placement within this group. We also assume, following Zaher (1999), that the other Neotropical genera Crisantophis , Diaphorolepis , Emmochliophis , Enuliophis , Enulius , Hydromorphus , Nothopsis , Rhadinophanes Synophis , and Tantalophis which have a dipsadid hemipenial morphology, belong within Dipsadidae , and we place them here incertae sedis.

Guo et al. (2009) and He et al. (2009) have shown convincingly that the genus Thermophis Malnate, 1953 is more closely related to the Dipsadidae than it is to any other colubroid clade. However, a more thorough analysis of the phylogenetic affinities of Thermophis is still needed in order to clearly place this genus in respect to the Dipsadidae . Meanwhile, we include Thermophis Malnate, 1953 in the Dipsadidae as incertae sedis. Finally, the poorly known genera Cercophis , Lioheterophis , Sordellina , and Uromacerina that present a dipsadid hemipenial morphology and were considered by Zaher (1999) as being Xenodontinae incertae sedis are here included in the Dipsadidae incertae sedis.

Dipsadidae incertae sedis: Cercophis Fitzinger, 1843 ; Crisantophis Villa, 1971 ; Diaphorolepis Jan, 1863 ; Emmochliophis Fritts & Smith, 1969 ; Enuliophis Mc-Cranie & Villa, 1971; Enulius Cope, 1871 ; Farancia Gray, 1842 ; Heterodon Latreille (in Sonnini & Latreille), 1801; Hydromorphus Peters, 1859 ; Lioheterophis Amaral, 1934 ; Nothopsis Cope, 1871 ; Rhadinophanes Myers & Campbell, 1981 ; Sordellina Procter, 1923 ; Synophis Peracca, 1896 ; Tantalophis Duellman, 1958 ; Thermophis Malnate, 1953 ; Uromacerina Amaral, 1930 ; Xenopholis Peters, 1869 .

SUBFAMILY CARPHOPHIINAE new subfamily (Clade 29)

Diagnosis: (88%, 4). Hemipenes slightly bilobed to unilobed and noncapitate; sulcus spermaticus dividing distally, within the capitulum ( Myers, 1974; Cadle, 1984b; Zaher, 1999).

Content: Carphophis Gervais (in D’Orbigny), 1843 (type-genus of the subfamily); Contia Girard (in Baird & Girard), 1853; Diadophis Girard (in Baird & Girard), 1853.

Comments: Because Carphophis , Contia and Diadophis form a strongly supported clade that is also corroborated by derived hemipenial evidence, we here include them in a new subfamily Carphophiinae . Whether Farancia and Heterodon belong to this subfamily is a question that needs further investigation (see also comments under Dipsadidae ). The hemipenial morphology of Carphophiinae new subfamily ressembles the one of Dipsadinae , but differs in an important detail, namely the lack of capitation on the lobes.

For the sake of stability of the shark family name Heterodontidae Gray, 1851 , the name Heterodontinae Bonaparte, 1845, used by Vidal et al. (2007) for the North American xenodontines (including Heterodon and Farancia ), should be avoided ( Rossman & Wilson, 1964).

SUBFAMILY DIPSADINAE Bonaparte, 1838 (Clade 31)

Dipsadina Bonaparte, 1838: 392.

Type-genus: Dipsas Laurenti, 1768 .

Diagnosis: (74%, 7). Hemipenes unilobed or with strongly reduced bilobation; hemipenes unicapitate; sulcus spermaticus dividing distally, either at the base of, or within, the capitulum ( Myers, 1974; Cadle, 1984b; Zaher, 1999).

Content: Adelphicos Jan, 1862 ; Amastridium Cope, 1861 ; Atractus Wagler, 1828 ; Chapinophis Campbell & Smith, 1998 ; Chersodromus Reinhardt, 1860 ; Coniophanes Hallowell (in Cope), 1860; Cryophis Bogert & Duellman, 1963 ; Dipsas Laurenti, 1768 ; Eridiphas Leviton & Tanner, 1960 ; Geophis Wagler, 1830 ; Hypsiglena Cope, 1860 ; Imantodes Duméril, 1853 ; Leptodeira Fitzinger, 1843 ; Ninia Girard (in Baird & Girard), 1853; Plesiodipsas Harvey, Fuenmayor, Portilla & Rueda-Almonacid, 2008 ; Pliocercus Cope, 1860 ; Pseudoleptodeira Taylor, 1938 ; Rhadinaea Cope, 1863 ; Sibon Fitzinger, 1826 ; Sibynomorphus Fitzinger, 1843 ; Tretanorhinus Duméril, Bibron & Duméril, 1854 ; Trimetopon Cope, 1885 ; Tropidodipsas Günther, 1858 ; Urotheca Bibron (in de la Sagra), 1843.

Comments: Hemipenial morphology varies among this diverse group and the level of generality of the hemipenial synapomorphies we cite should be reviewed as more taxa are surveyed (see Zaher, 1999 for discussion). A simple sulcus spermaticus is present in some dipsadines as a further derived condition.

We refrain from defining tribes within Dipsadinae in the present analysis since we have sampled little of the diversity within this large group. However, there are indications from both molecular ( Cadle, 1984b; Mulcahy, 2007) and morphological ( Peters, 1960; Myers, 1974; Cadle, 1984b, 2007; Oliveira et al., 2008; Vidal et al., 2000) data for a monophyletic Leptodeirini including at least the genera Leptodeira and Imantodes and a monophyletic Dipsadini including at least Dipsas , Sibon , Sibynomorphus , and Tropidodipsas . However, much more work will be required to confidently resolve the relationships among the other species of this diverse group (> 200 species).