Chiasmocleis hudsoni

Peloso, Pedro L. V., Sturaro, Marcelo José, Forlani, Mauricio C., Gaucher, Philippe, Motta, Ana Paula & Wheeler, Ward C., 2014, Phylogeny, Taxonomic Revision, And Character Evolution Of The Genera Chiasmocleis And Syncope (Anura, Microhylidae) In Amazonia, With Descriptions Of Three New Species, Bulletin of the American Museum of Natural History 2014 (386), pp. 1-1 : 76-78

The Chiasmocleis hudsoni Clade: Taxonomy and Evolution

TAXONOMY: The topology of this clade, is substantially different from that of de Sá et al. (2012). Their specimen of C. carvalhoi (as Syncope carvalhoi in their analysis; see fig. 2) was found at a basal position, and sister to all remaining species in the clade (which also included C. bassleri in their results), while we recovered that same specimen nested within our samples of C. antenori . The two specimens labeled as Syncope sp. by de Sá et al. (2012) were found here to be part of C. carvalhoi . We have included three specimens of C. tridactyla , from Leticia, Colombia —this species was not sampled by de Sá et al. (2012). We have also named a new species, which is included in this clade ( C. haddadi ).

EVOLUTION: A few members of this clade show an advanced degree of miniaturization, which includes lost of vertebrae and digits ( Silva and Meinhardt, 1999). Reproductive biology characters also are of great interest as at least one species has a derived reproductive mode, with tadpoles developing inside bromeliads. Direct development has been postulated in other members of the clade as well, ( Krügel and Richter, 1995; Moravec and Köhler, 2007), but to our knowledge never confirmed by empirical observations.

Unfortunately, limited data on osteology, as well as missing data on ecology and behavior precludes any detailed analysis of evolutionary trend in the clade. Fieldwork directed to collect data on reproduction and behavior of species in this clade can prove useful for understanding the evolution of reproductive biology of this very interesting lineage of frogs.

PHENOTYPIC VARIATION

Our results revealed some amount of variation in morphology (see species accounts) and advertisement call parameters (see call descriptions under each species account) in Amazonian and Guiana populations of Chiasmocleis . This is also true for non-Amazonian species of the genus ( Caramaschi and Cruz, 1997; Cruz et al., 2007a,b). Thus, it is extremely important that population variation among populations of described species be studied for a more accurate definition of diagnostic characters and species boundaries ( Frost et al., 1998). The lack of a more complete understanding of variation may lead to inaccuracies in diagnoses and species recognition. As an example, the comparative table presented by Funk and Cannatella (2009: 40, table 1) lacks most of the species of Chiasmocleis and the sample of characters is very limited, rendering it unsuitable for diagnosing any species of Chiasmocleis (their table was likely based solely on the literature, which is limited for many Chiasmocleis species ). Although considerably more complete (20 species represented), the table presented by Morales and McDiarmid (2009: 76, table 1) is also not very reliable. Although they compared several species, the authors do not present a list of material examined, and therefore it is impossible to assess whether the table was based on the direct comparison of specimens or on the literature. Furthermore, inaccurate information is given such as: (1) the absence of toe discs in C. jimi (considered here a synonym of C. hudsoni ; toe discs present in most specimens examined and also reported in the original description, Caramaschi and Cruz, 2001); (2) dorsal pattern uniform in C. bassleri and C. shudikarensis (clearly not uniform in several specimens of C. bassleri , e.g., pl. 4, and in C. shudikarensis , e.g., pl. 7); (3) dorsal dermal spines absent in C. shudikarensis (conspicuously present in most males examined, indeed absent in most females). These inaccuracies render such comparative tables less reliable and prone to misidentifications. We regard both the tables provided by Funk and Cannatella (2009) and Morales and McDiarmid (2009) as of limited utility for any purpose regarding the taxonomy of Chiasmocleis and they should be avoided for the identification of species in the genus.

Many species of Chiasmocleis look alike, and the addition of characters is crucial for the progress of taxonomy in the group. We point out that although the degree of webbing on toes, development of fringes, presence/ absence of femoral lines, presence/absence and distribution of dermal spines, presence/ absence of an inguinal blotch, and general color pattern are useful characters, they should be carefully evaluated and used with caution. Sexual dimorphism—as well as ontogenetic variation—in toe webbing and the presence/distribution of dermal spines should be considered when comparing species. Fringes and dermal spines could be related to reproductive activity and also show some populational variation. Color patterns have been shown to change ontogenetically in several amphibian species including some species of the Microhylidae ( Kraus and Allison, 2009) , and the nature of this sort of variation within Chiasmocleis is, to this point, obscure.

Advertisement calls are also a powerful source of information for anuran systematics and this is no different with the Microhylidae . Despite the similar structure of most Chiasmocleis advertisement calls, usually composed of a series of multipulsed notes ( Santana et al., 2009; but see Santana et al., 2012, for the peculiar call of C. mantiqueira ), many diagnostic characters can still be extracted from analyses of well-recorded advertisement calls (i.e., call rate, number of pulses, frequency data).

CHARACTER EVOLUTION

Optimization of phenotypic characters in the phylogeny of Chiasmocleis suggests that all characters evaluated have complex histories, with multiple transformations involved (e.g., multiple losses of dermal spines, and multiple appearances of the femoral line).

The optimization of dermal spines and degree of toe webbing were unambiguous and needed three and four steps, respectively (fig. 49). The presence of dermal spines in Chiasmocleis is apparently plesiomorphic and was lost three times, independently, in the group (fig. 49A). Although the presence of extensive webbing is widespread in Anura , including many other microhylids, the absence of extensive webbing is the plesiomorphic state in Chiasmocleis with four independent appearances of webbing in the group (fig. 49B). The amount of webbing in Chiasmocleis may be related to the ability of males for swimming and/or floating on water, but additional field observations will corroborate or refute this prediction.

Evolutionary history of the femoral lines is more complex and could not be unambiguously optimized. The optimization of this character requires at least four steps and four equally parsimonious alternative scenarios were found (fig. 50). These alternative scenarios are as diverse as the postuation of a single origin with three subsequent losses (fig. 50A) to four independent appearances of the femoral line line (fig. 50D). Intermediate scenarios, involving independent appearances and reversals, are shown in figure 50B–C. The function of the femoral line is not known. Although a similar line is present in other gastrophrynine microhylids (e.g., Hamptophryne boliviana ) the absence of the femoral line is the plesiomorphic state in Chiasmocleis .

In an attempt to understand the evolution of reproductive modes in Chiasmocleis , we optimized egg clutch size on the tree. Although information is missing for a few species, a single event of decrease in number of eggs per clutch is postulated on the branch leading to C. magnova , C. antenori , C. carvalhoi , and C. tridactyla (information on clutch size is not available for C. tridactyla ; fig. 51).

Mapping of additional reproductive characters on the tree suggest that a complex evolutionary scenario played out in the C. hudsoni clade (fig. 51). In addition to reduction in clutch size, endotrophic but freeswimming tadpoles were reported for C. antenori ( Krügel and Richter, 1995) . The presence of unpigmented eggs in C. carvalhoi and C. magnova has been associated to the presence endotrophic larvae (perhaps even direct development) in those species (see Nelson, 1975; Krügel and Richter, 1995; Moravec and Köhler, 2007), but this was never confirmed by field or laboratory observations. The amount of missing data on reproductive behavior for Chiasmocleis , and especially in this miniaturized species, hinders a better understanding of the transformation series involved in the appearance of endotrophic tadpoles and, potentially, direct development in the group.

Miniaturization and ‘‘terrestrialization’’ (i.e., evolution of endotrophic tadpoles or direct development) have been associated with higher rates of diversification and evolutionary success in frogs, including cophyline ( Andreone et al., 2005) and asterophryine ( Zweifel, 1972) microhylids, although empirical tests did not find this to be correct in all cases ( Gomez-Mestre et al., 2012; Zimkus et al., 2012). It appears that this is also not the case for New World microhylids. Endotrophic tadpoles are present at least in Chiasmocleis (see above), Myersiella ( Izecksohn et al., 1971: monotypic), and Synapturanus ( Menin et al., 2007: three known species). Although the low number of species can be a result of poor taxonomic knowledge (e.g., we are aware of additional Myersiella and Synapturanus species awaiting description: P.L.V.P., personal obs.) we do not expect the number of species to increase drastically so as to represent hyperdiverse clades. Notwithstanding the fact that data on ecology are missing for key taxa (fig. 51), it seems clear to us that miniaturization and terrestriality (both conspicuous characteristics of species in the C. hudsoni clade) did not have a major impact in the diversification of Chiasmocleis . At any rate, only when we have information on egg development for all species in the C. hudsoni clade will it be possible to assess the impact of this novelty in the evolution of the group.