Fritziana, Mello-Leittao, 1937

Folly, Manuella, Kirchmeyer, Juliana, Bezerra, Andressa M., Carvalho-e-Silva, Sergio P. de & Trueb, Linda, 2022, The egg-brooding frogs Fritziana Mello-Leit ˜ ao, 1937 and Flectonotus Miranda-Ribeiro, 1926 (Amphibia: Anura): osteology and putative synapomorphies for hemiphractid frogs, Zoologischer Anzeiger 298, pp. 170-197 : 187-194

3.4. Phenotypic characters in Fritziana and Flectonotus

Mendelson et al. (2000; see also Castroviejo-Fisher et al. 2015) coded 40 cranial characters in their study of the phylogenetic relationships of marsupial frogs, including for Fritziana and Flectonotus . We recoded some of those characters based on our study and traced how they evolved in the family phylogenetic tree. We also propose eight new characters from skeletal (e.g., skull, pectoral girdle, hands) morphology for Fritziana , Flectonotus , and related groups.

3.4.1. Character 1

Ventral skull, parasphenoid, extension of anterior terminus of cultriform process (Character 5 of Mendelson et al. 2000) (0) posterior to orbitonasal foramina; (1) coincident with the level of orbitonasal foramina; (2) anterior to orbitonasal foramina.

The state of this character in both Fritziana and Flectonotus is plesiomorphic, with the cultriform process extending to the level of orbitonasal foramina, except for Fr. fissilis (State 1). The anterior terminus posterior to orbitonasal foramina (State 0) is a putative synapomorphy of Cryptobatrachus ( Fig. 8A ). Hemiphractus fasciatus also has this character state. Extension of the anterior terminus anterior to orbitonasal foramina is the ancestral state for the Gastrotheca + Hemiphractus clade, and it is also present in F. fissilis .

3.4.2. Character 2

Ventral skull, anterolateral extent of anterior process of vomer (modified Character 14 of Mendelson et al. 2000) (0) articulating with the maxilla; (1) articulating with the maxilla and premaxilla; (2) articulating with the premaxilla; (3) no articulation present.

This character was previously recovered as homoplastic for hemiphractid frogs ( Castroviejo-Fisher et al. 2015; Mendelson et al. 2000). The reconstruction of this character is ambiguous for the ancestor of the family. Lack of an articulation of the anterior process of vomer with the maxilla and premaxilla (State 3) is present in the ancestor of Flectonotus and it is a putative synapomorphy of the genus ( Fig. 9A ). It is also present in Fr. tonimi , Fr. ohausi , and Fr. goeldii . Fritziana izecksohni has State 1, with the anterior process of vomer articulating with both the maxilla and premaxilla. Despite the great variation in this character states observed in species of Fritziana , the ancestral condition for the genus is the anterior process articulating with the premaxilla—a condition that is retained only in Fr. fissilis (State 2). The anterior process articulating only with maxilla (State 0) is present in some species of Cryptobatrachus and in the ancestor of the clade Gastrotheca + Hemiphractus .

3.4.3. Character 3

Ventral skull, length of postchoanal process of vomer (Character 16 of Mendelson et al. 2000) (0) short, extending around less than half of choana; (1) long, extending around more than half of choana; (2) minute, extending only to the median edge of choana, posteriorly parallel to the skull axis.

Previous tests of this character recovered it as homoplastic for the family ( Castroviejo-Fisher et al. 2015; Mendelson et al. 2000). Although the condition of this character is unknown for some species of Fritziana , Cryptobatrachus , and Stefania , the presence of a long postchoanal process (State 1) is plesiomorphic for the family and is conserved in both Flectonotus and Fritziana ( Fig. 9B ). The shorter processes (States 0 and 2) are present in some species of Gastrotheca and Hemiphractus .

3.4.4. Character 4

Ventral skull, medial contact of vomers (modified Character 17 of Mendelson et al., 2000) (0) not in contact, broadly separated by a distance greater than the length of the palatine processes of premaxillae (1) not in contact, narrowly separated by a distance equal to the length of the palatine processes of premaxillae; (2) in contact.

Ponssa (2008) coded this character as vomers separated, vomer contiguous or in contact, recovering it as homoplastic. Broadly separated vomers (State 0) is plesiomorphic in Hemiphractidae . This state is retained in most species of Fritziana and in Flectonotus pygmaeus . Vomers narrowly separate (State 1) occurs independently in Fr. fissilis and Fl. fitzgeraldi ( Fig. 10C,F. H ); however, the state of this character is unknown for Fr. mitus , Fr. sp. CS1 and Fr. sp. CS2. Articulating vomers (State 2), presenting no separation, evolved independently in the ancestor of Cryptobatrachus , and in some species of Hemiphractus and Gastrotheca .

3.4.5. Character 5

Ventral skull, orientation of dentigerous process of vomers in relation to the transversal plan (0) diagonal; (1) parallel.

In the ancestral condition, the dentigerous process of the vomers is

Table 2 (continued)

Bone/cartilage Process Fritziana Flectonotus Cryptobatrachus Gastrotheca Stefania Hemiphractus same width in its same width in its same width in its same width in its same width in its narrowly distally entire length entire length entire length entire length, or entire length narrowly distally posteromedial terminates anterior terminates at terminates anterior terminates anterior terminates anterior terminates at process to foramen magnum foramen magnum to foramen magnum or at foramen to foramen magnum foramen magnum magnum Vomers anterior not articulating with not articulating with not articulating articulating or not articulating with articulating with process maxillae maxillae with maxillae with maxillae maxillae maxillae pre- and around the same around the same around the same around the same postchoanal around the same postchoanal length, or the length, or the length length, or the slightly longer than length or processes prechoanal slightly prechoanal slightly prechoanal slightly the prechoanal prechoanal is longer than the longer than the longer than the slightly longer postchoanal postchoanal postchoanal than the postchoanal dentigerous straight series straight series arched series straight series straight series straight series process dentigerous horizontal or horizontal horizontal horizontal or horizontal horizontal process diagonal orientated orientated orientated diagonal orientated orientated orientated dentigerous 5–7 teeth each 3–5 teeth each 11 teeth each 3–9 teeth each 9 teeth each 0–2 teeth each process

– not in contact, not in contact, not in contact, not in contact, in contact one not in contact,

broadly separated by broadly separated by narrowly separated broadly separated by another narrowly a distance greater a distance greater with one another, a distance greater separated with one than the length of than the length of by a distance equal than the length of another, by a the palatine the palatine to the length of the the palatine distance equal to processes of the processes of the palatine processes processes of the the length of the premaxillae; or premaxillae; or of the premaxillae; premaxillae; or palatine processes narrowly separated, narrowly separated, or in contact one narrowly separated, of the premaxillae by a distance equal by a distance equal another by a distance equal to the length of the to the length of the to the length of the palatine processes of palatine processes of palatine processes of the premaxillae premaxillae premaxillae or in contact one another Premaxillae alary process the distal tips parallel along the parallel along the parallel or distal tips parallel along the parallel along the diverge from one entire length entire length diverge from one entire length entire length another another Maxillae preorbital present or absent present present present or absent absent present process postorbital absent absent absent present or absent absent present process Hyoid alary process a distal expansion same width in its With a distal a distal expansion with the same with the same apparatus may be present or entire length expansion may be present or width in its entire width in entire not not length length posterolateral present present present present absent absent process posterolateral small, extending less long, extending long, extending small, extending less – –

process than 1/5; moderate almost 2/3 of the almost 2/3 of the than 1/5; moderate extending between postero-medial postero-medial extending between

1/5 and 1/; or long, process of the hyoid process of the hyoid 1/5 and 1/; or long,

extending almost 2/ plate plate extending almost 2/

3 of the postero- 3 of the posteromedial process of the medial process of hyoid plate hyoid plate posteromedial posterior ends posterior ends not posterior ends not posterior ends posterior ends not posterior ends not process expanded expanded expanded expanded or not expanded expanded Laryngeal arytaenoids very small, with less small, around 2/3 of small, around 2/3 of very small, with less small, around 2/3 very small, with cartilages than half of the the lenght of the the lenght of the than half of the of the lenght of the less than half of the lenght of the postero-medial postero-medial lenght of the postero-medial lenght of the postero-medial process process postero-medial process postero-medial process; or small, process; small, process; or small,

around 2/3 of the around 2/3 of the around 2/3 of the lenght of the lenght of the lenght of the postero-medial postero-medial postero-medial process process; moderate, process with the same length as the posteromedial process; or bigger than the lenght of the postero-medial process Vertebral transverse III> IV = V = VI = III> IV = V = VI = III> IV = V = VI = III> IV = V = VI = II <IV = V = VI = III> IV> V> VI> column process length VII = VIII = II VII = VIII = II VII = VIII = II VII = VIII = II or III VII = VIII = III VII> VIII> II

= IV> V = VI = VII

= VIII = II Pectoral girdle omosternum

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Table 2 (continued)

parallel to the transversal plan (State 1) ( Fig. 10B ). Diagonal dentigerous processes (State 0) evolved independently in Fr. tonimi and Fr. goeldii , and in some species of Gastrotheca .

3.4.6. Character 6

Lateral skull, preorbital process of maxillae (Character 19 of Mendelson et al. 2000) (0) present, distinct from pars facialis; (1) absent.

The preorbital process is small and extends dorsally from the maxilla just anterior to the orbit ( Maglia 1998). All species of Fritziana , except Fr. goeldii , have a short dorsal process (preorbital) of the pars facialis, extending toward the maxillary process of the nasal. Presence of preorbital process (State 0) is plesiomorphic for hemiphractid frogs and it is retained in Fritziana and Flectonotus . A distinct preorbital process is absent (State 1) in the ancestor of the clade formed by Gastrotheca + Hemiphractus , as well as in Fr. goeldii ( Fig. 11A ).

3.4.7. Character 7

Ventral skull, extension of anterior terminus of the quadratojugal (modified Character 23 of Mendelson et al. 2000) (0) articulating with maxilla; (1) not articulating with maxilla, reaching less than half of the length of the anterior process of pterygoid; (2) not articulating with maxilla and coincident with the midlength of the anterior ramus of the pterygoid.

Mendelson et al. (2000) coded the quadratojugal as articulating or not with maxilla. Later, Castroviejo-Fisher et al. (2015) recovered absence of articulation between maxillae and quadratojugal as homoplastic for Fritziana (Character 23, 0 → 1) and in Flectonotus pygmaeus . We observed species of Flectonotus with longer quadratojugals than those of Fritziana ; therefore, we recode this character as the extension of the anterior terminus of the quadratojugal.

Anterior terminus of the quadratojugal articulating with the maxilla (State 0) is plesiomorphic for hemiphractid frogs. A short quadratojugal that does not articulate with the maxilla (State 1) is a putative synapomorphy of Fritziana ; however, this character state is unknown for Fr. mitus , Fr. sp. CS1, and Fr. sp. CS2. Presence of a quadratojugal not articulating with maxilla and with its terminus coincident with the midlength of the anterior ramus of the pterygoid is a putative synapomorphy of Flectonotus (State 2; Fig. 11B ).

3.4.8. Character 8

Dorsal skull, nasal size (modified Character 32 of Mendelson et al. 2000) (0) small nasals, leaving a wide medial separation; (1) moderate nasals, leaving a moderated medial separation; (2) large nasals, leaving a narrow medial separation; (3) large nasals articulating, without separation.

Duellman & Gray (1983) noticed the difference in the separation of the nasal between species of Fritziana and Flectonotus , and proposed that the broadly separated nasals of Flectonotus and the large nasals nearly in contact with the anterior part of the sphenethmoid of Fritziana to be diagnostic features for each genus. Medial articulation of nasals was previously coded as absent or present ( Mendelson et al. 2000); however, we observed that the hemiphractid nasals vary more in size than indicated by previous authors. Herein, large nasals with a narrow medial separation (State 2) is plesiomorphic for the family, and occurred independently in G. orophylax , G. litonedis and G. peruana . Castroviejo-Fisher et al. (2015) recovered absence of a nasal articulation with the maxilla as diagnostic for species of Fritziana . The ancestor of Fritziana retained the plesiomorphic state (State 2). Large nasals without medial separation appeared in the ancestor of the clade composed by Gastrotheca and Hemiphractus . The presence of a moderate gap between moderately sized nasals (State 1) occurred independently in Fr. tonimi and Fr. ohausi , and in some species of Gastrotheca ( Fig. 12A ). A presence of a wide gap between small slender nasals (State 0) is a putative synapomorphy of Flectonotus .

3.4.9. Character 9

Dorsal skull, exposition of frontoparietal fenestra (modified Character 35 of Mendelson et al. 2000) (0) narrow fenestra, less than one fifth of sphenethmoid width; (1) moderate fenestra, one third to less than half of the sphenethmoid width; (2) broad fenestra, half or more of the sphenethmoid width; (3) fenestra narrow anteriorly with a small exposition posteriorly; (4) absent fenestra.

Mendelson et al. (2000) coded the medial articulation of frontoparietals as absent, present only posteriorly, or complete. We observed that the frontoparietal fenestra might be narrow, moderate, or broad; therefore, we recoded the character.

Presence of a moderate-sized fenestra (State 1) is plesiomorphic for the family and is retained in Fritziana . Presence of a narrow fenestra (State 0) is a putative synapomorphy of Flectonotus . It also evolved independently in some species of Gastrotheca . Presence of a broad fenestra (State 2) evolved independently in Fr. ohausi and in Cryptobatrachus sp. ( Fig. 12B ). Presence of broadly articulated frontoparietals with a small, posterior fenestra (State 3) is present in Stephania scalae and in the ancestor of the clade Gastrotheca + Hemiphractus . Complete articulation and absence of a fenestra (State 4) is also present in some species of this clade.

3.4.10. Character 10

Dorsal skull, length of squamosal zygomatic ramus (modified Character 39 of Mendelson et al. 2000) (0) reduced, very distant from reaching the level of the maxillary arcade; (1) short, almost reaching the level of the maxillary arcade; (2) medium, reaching the maxillary arcade; (3) long, articulating with the postorbital process of maxilla; (4) long, extending beyond the postorbital process of maxilla.

Mendelson et al. (2000) proposed four possible states of zygomatic ramus (short; long, not articulating with maxilla; long, articulating only with postorbital process of maxilla and extending beyond dorsal margin of postorbital process to articulate with body of maxilla). However, we found that these states are not mutually exclusive—i.e., two different states can be found in the same species. This occurs in some species of Gastrotheca , in which the zygomatic ramus may be long and articulate only with postorbital process of maxilla and which also may extend beyond the dorsal margin of the postorbital process to articulate with the body of maxilla. To clarify these characters states, we propose some new states. Mendelson et al. (2000) recovered such states as homoplastic for hemiphractid frogs (also see Castroviejo-Fisher et al. 2015).

The reconstruction of this character is ambiguous for the ancestor of the family. The presence of a reduced zygomatic ramus very distant from reaching the maxilla arcade (State 0) emerged in the ancestor of the clade Flectonotus + Cryptobatrachus . It also occurs in four species of Hemiphractus and G. walkeri ( Fig. 13A ). The presence of a medium zygomatic ramus that reaches the maxillary arcade (State 2) is present in the most recent common ancestor of Fritziana , decreasing in size (short size; State 1) in Fr. goeldii and Fr. ohausi .

3.4.11. Character 11

Dorsal skull, extension of otic ramus of squamosal (0) not articulating with crista parotica; (1) articulating with crista parotica.

The reconstruction of this character is ambiguous for the ancestor of the family. The lack of an articulation between the otic ramus of squamosal and crista parotica (state 0) occurs in two species of Fritziana ( Fr. goeldii and Fr. tonimi ), in both species of Flectonotus , as well as in some species of Gastrotheca ( Fig. 13B ). The presence of an articulation between the otic ramus and crista parotica (State 1) is present in Fr. fissilis , S. scalae , and the most recent common ancestor of Gastrotheca .

3.4.12. Character 12

Pectoral girdle, clavicles orientation (0) straight, inclined anteriorly at ~15 ◦ angle; (1) straight, inclined anteriorly at ~30 ◦ angle; (2) slightly concave, inclined at ~45 ◦ from the glenoid fossa.

The reconstruction of this character is ambiguous for the ancestor of the family. Straight clavicles inclined anteriorly at ~15 ◦ angle (State 0) evolved independently in the ancestor of the clade Flectonotus + Cryptobatrachus , and in some species of Hemiphractus and Gastrotheca ( Fig. 14A ). Possession of clavicles inclined anteriorly at ~30 ◦ angle (State 1) occurs in Fr. tonimi , Fr. ohausi , and Fr. ulei (not included in the phylogenetic study), and in some species of Gastrotheca .

3.4.13. Character 13

Pectoral girdle, omosternum shape (0) oval; (1) triangular; (2) anterior apex slightly dilated; (3) anterior apex extremely dilated, with an anvil shape.

The omosternum is a midventral element lying anterior to the procoracoids and clavicles ( Trueb 1973). The presence of an anterior and slightly dilated omosternum (State 3) is plesiomorphic for the family and retained in Flectonotus species. The presence of an oval omosternum (State 0) is a putative synapomorphy of Fritziana , although the state of this character is unknown for Fr. mitus , Fr. sp. CS1, and Fr. sp. CS2. The presence of an omosternum with an extremely dilated anterior apex (State 3) is a putative synapomorphy of Cryptobatrachus ; however, the state of this character is unknown in C. remotus ( Fig. 14B ).

3.4.14. Character 14

Pectoral girdle, sternum, ossification extension (0) half sternum ossified (1) ossified only along peripheral border of anterior half of sternum; (2) not ossified.

Usually, the sternum is a flat, cartilaginous element associated with the posteromedial part of the pectoral girdle; it may be calcified or ossified ( Trueb 1973). The absence of sternal ossification (State 2) is plesiomorphic in the family and retained in the Fritziana species. Peripheral ossification of sternum (State 1) occurs in both species of Flectonotus and their ancestor ( Fig. 15A ). A partially ossified sternum ossified (State 0) is present in G. monticola and in Cryptobatrachus fuhrmanni .

3.4.15. Character 15

Hand, relative lengths of Fingers II and III (0) Finger II longer than Finger III; (1) Fingers II and III equal in length; (2) Finger II shorter than Finger III.

Given the loss of Finger I in anurans ( Fabrezi & Alberch 1996), the arrangement of the carpal elements in hemiphractids is the C-morphology described by Fabrezi (1992), comprising the ulnare,

radiale, fused Distal Carpal 5-4-3, Distal Carpal 2, and Element Y. Lengths of Fingers II and III equal (State 1) is plesiomorphic for the family and retained in Fritziana species (State 1). Finger II longer than Finger III (State 0) occurs in Flectonotus and Hemiphractus , whereas the inverse (State 2) is a putative synapomorphy of Cryptobatrachus ( Fig. 15B ).

Figures

Fig. 8. Parsimonious optimization onto Echevarría et al. (2021) phylogenetic hypothesis: extension of anterior terminus of cultriform process of parasphenoid. See Supplemental Material for the complete matrix, including outgroups. Gray represents unknown condition.

Fig. 9. Parsimonious optimization onto Echevarría et al. (2021) phylogenetic hypothesis (A) anterolateral extent of anterior process of vomer (B) lenght of postchoanal process of vomer. See Supplemental Material for the complete matrix, including outgroups. Gray represents unknown condition.

Fig. 10. Parsimonious optimization onto Echevarría et al. (2021) phylogenetic hypothesis (A) medial contact of vomers (B) orientation of dentigerous process of vomers. See Supplemental Material for the complete matrix, including outgroups. Gray represents unknown condition.

Fig. 11. Parsimonious optimization onto Echevarría et al. (2021) phylogenetic hypothesis (A) preorbital process of maxilla (B) extension of anterior terminus of quadratojugal. See Supplemental Material for the complete matrix, including outgroups. Gray represents unknown condition.

Fig. 12. Parsimonious optimization onto Echevarría et al. (2021) phylogenetic hypothesis (A) nasal size (B) exposition of frontoparietal fenestra. See Supplemental Material for the complete matrix, including outgroups. Gray represents unknown condition.

Fig. 13. Parsimonious optimization onto Echevarría et al. (2021) phylogenetic hypothesis (A) lenght of squamosal zygomatic ramus (B) extension of otic ramus of squamosal. See Supplemental Material for the complete matrix, including outgroups. Gray represents unknown condition.

Fig. 14. Parsimonious optimization onto Echevarría et al. (2021) phylogenetic hypothesis (A) clavicules orientation (B) shape of omostermum. See Supplemental Material for the complete matrix, including outgroups. Gray represents unknown condition.

Fig. 15. Parsimonious optimization onto Echevarría et al. (2021) phylogenetic hypothesis (A) ossification extension of sternum (B) relative length of Fingers II See Supplemental Material for the complete matrix, including outgroups. Gray represents unknown condition.