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COPEIA August 3 1988, No. 3 COPEIA August 3 Copria, 1988(3),pp. 527-543 Evolution of Marsupial Frogs (Hylidae: Hemiphractinae): Immunological Evidence Marsupial tree frogs (Hylidae: Hemiphractinae) share the unusual feature of females brooding eggs on the dorsum or in a dorsal pouch. Results of studies of albumin evolution in these frogs suggest that the generic lineages are ancient (Cretaceous),that a minimum of four species groups can be identified within the genus Gastrotheca and that the monotypic Amphignathodon should be placed in Gastrotheca. The results also support recent suggestions that direct development is the plesiomorphic reproductive mode in egg-brooding hylid frogs. The esti- mated times of divergence of various lineages coincide with major orogenic events in South America. Los sapos marsupiales (Hylidae: Hemiphractinae) se caracterizan por trans- portar las hembras 10s huevos en el dorso o en un saco dorsal. Los resultados del analisis de la evolution de las albuminas sugieren una divergencia cretacica para dicho genero. El genero monotipico Amphignathodon quizis deberia ser relocalizado con el genero Gastrotheca, dentro del cual se reconocen cuatro grupos de especies. Este arreglo estaria de acuerdo con recientes indicaciones por las cuales el desarrollo direct0 es un modo reproductivo plesiomorphico en 10s hylidos marsupiales. Las epocas estimadas de divergencia evolutiva coinciden con 10s grandes eventos orogenicos en Suramerica. TUDIES of albumin evolution have provid- the eggs hatch directly into froglets; there is no S ed evidence of relationships among taxa in free-living tadpole stage. In Flectonotus and Fritr- several anuran families over the past decade iana, the eggs hatch into advanced, nonfeeding (Maxson et al., 1982; Maxson, 1984; Maxson tadpoles that complete their development in a and Roberts, 1985). Because of their unusual few days in water in bromeliads or tree holes mode of reproduction, the approx. 60 species (Duellman and Gray, 1983). The free-living, of egg-brooding hylid frogs of the subfamily feeding tadpoles produced by some species of Hemiphractinae (including Amphignathodon- Gastrotheca have a lengthy development period tinae) have been the subject of several evolu- in ponds. tionary studies in recent years (Duellman and There seems to be a simple orthogenetic pro- Hoogmoed, 1984; Wassersug and Duellman, gression in the reduction of larval features of 1984; Duellman and Hillis, 1987). Frogs in this the oral morphology in Gastrotheca; thus, free- subfamily share a unique embryonic feature- living tadpoles have the most completely de- large, membranous, external gills that com- veloped mouthparts, whereas embryos of di- pletely (or partially) envelop the embryos, all of rect~developin~speciesof Gastrotheca'and other which develop on the dorsum of females (Cqp- genera of herniphractines have reduced mouth- tobatrachus, Hemzphractus, and Stejania) or in a parts (Wassersug and Duellman, 1984). These brood pouch on the dorsum of females (Am- authors suggested that the oral morphology of phzgnathodon, Flectonotus, Fritziana, and Gastro- direct-developing species of Gastrotheca can be theca). In Amphignathodon, Cryptobatrachus, Hemz- accounted for by simple truncation of the nor- phractus, Stejania, and most species of Gastrotheca, mal tadpole developmental program. Thus, the O 1988 by the iZmerican Society of Ichthyologists and Herpetologists 528 COPEIA, 1988, NO. 3 tadpole-producing species of Gastrotheca may monticola (I), G. nicefori (1) and G. pseustes (1). have evolved from lineages having direct de- Additionally, plasma or muscle tissue preserved velopment. A preliminary immunological study in phenoxyethanol (Maxson and Wilson, 1975) of Gastrotheca (Scanlan et al., 1980) showed that were used as albumin samples from 18 popu- direct development existed in several lineages lations of G. pseustes, seven populations of G. of Gastrotheca; thus, either direct development riobambae, 17 additional species of Gastrotheca, or the free-living larval condition may have aris- Flectonotus jitzgeraldi, Fritziana goeldii, Hemi- en independently several times in the genus. phractus bubalus, H.fasciatus, Stefania mansi and A cladistic analysis of allozymes of the high- S. ginesi (see Appendix 1 for museum numbers Andean groups of Gastrotheca (Duellman and for voucher specimens and locality data). Hillis, 1987) supported the recognition of Several frogs from the same population were northern (G. plumbea) and southern (G. marsu- pooled in order to obtain sufficient plasma for piata) groups of high-Andean Gastrotheca, as producing antisera. Otherwise, all albumins used suggested on the basis of immunological evi- in micro-complement fixation (MC'F) tests were dence by Scanlan et al. (1980). Furthermore, maintained as individual samples. Several in- the allozymic analysis showed that plesiomor- dividuals from randomly selected populations phic alleles were shared by the two montane of G. riobambae and G. pseustes were tested ini- groups and the lowland species having direct tially to ascertain levels of intrapopulational development. This reproductive mode occurs variation in albumin. In all cases, immunolog- in most of the species in the G. marsupiata group ical distances (ID) from different individuals and in two members of the G. plumbea group. varied by only 1 or 2 units, the same amount However, allozymic data suggest that tadpole of variation reported in other studies (Maxson, production is plesiomorphic in the G. plumbea 1981; Maxson and Svzmura. 1984). The sam- group and that direct development in G. oro- ples of G. riobambae ind G. pseustes'used as an- phjlax and G. plumbea is derived. Thus, the ques- tigens for comparisons in Tables 1, 3-4 were tion remains: In the egg-brooding hylid frogs, the homologous populations used for produc- is direct development primitive or derived? In ing:" antisera. order to test these alternatives, we have ex- All antisera were used in the quantitative mi- panded our earlier immunological study (Scan- cro-complement fixation (MC'F) assay (Cham- Ian et al., 1980) to include all genera of hemi- pion et al., 1974; Maxson and Maxson, 1986) phractine frogs and many additional species of to estimate albumin evolution in these fro~s.0 Gastrotheca. In so doing, we also have examined Data are reported as immunological distances the immunological relationships among the taxa (ID).~, For albumin it has been determined that in light of their taxonomy and biogeography. one unit of ID is approximately equivalent to one amino acid difference between the albu- mins compared (Maxson and Wilson, 1975; Maxson and Maxson, 1986) and that approx. Albumin antisera were prepared according to 10 such substitutions accumulate every 5.5-6 established procedures (Maxson et al., 1979). million years of lineage independence (Wilson For species represented by a small sample, only et al., 1977). Divergence times are reported as one or two (rather than the standard three) rab- ranges calculated by multiplying the smallest ID bits were immunized to elicit antisera. The by 0.55 and the largest ID by 0.60 so as to give nunl'uer uf rabbits used for antisera production the broadest time range possible. Sarich (1985) is indicated parenthetically in the following list. reevaluated the calibration of the albumin mo- Comparative studies of antisera from single vs lecular clock in some placental mammals (based multiple rabbits indicate little variation among on quantitative precipitin data, not MC'F), but rabbits in estimates of albumin immunological we choose to use the former calibration because distances (Maxson, 1981; Busack et al., 1988). it is based on MC'F data, includes more exten- In addition to the antisera (to G. excubitor, G. sive vertebrate comparisons, and includes data marsupiata, G. ochoai, G. orophjlax, and G, rio- on diverse groups of anurans. bambae) used by Scanlan et al. (1980), the fol- The tree (Fig. 1) is a consensus of two trees, lowing antisera were prepared: Cryptobatrachus each constructed from averages of reciprocal fuhrmanni (2), Flectonotus pjgmaeus (I), Gastro- ID presented in Tables 1 (experimental data) theca argenteovirens (I), G. dendronastes (3), G. and 2 (adjusted data). Each tree was drawn using (Amphignathodon)guentheri(3), G. longipes (3), G. a modification of Farris' (1972) Wagner tree DUELLMAN ET AL.-MARSUPIAL FROG EVOLUTION algorithm. Because the variance in the estimat- ported by Scanlan et al. (1980). In those in- ed ID increases more rapidly than linearly with stances where the ID are not identical to those increasing ID (Maxson and Maxson, 1986), only reported earlier, the new ID are the result of the phylogenetically closest lineages are used to work that has been repeated using new individ- calculate limb lengths for the branches on the uals, or the reactions have been attempted at tree. This contrasts to the methods of Farris higher ID. For example, we used a different (1972) and Fitch and Margoliash (1967) where- sample of G. argenteouirens to prepare antisera in averages of all outside lineages generally are than that studied in 1980, and we report an ID used to calculate limb lengths. Our method pro- of 8 to G. orophylax, compared to the ID of 6 vides results that incorporate less "noise" than reported previously. The major discrepancy is the use of global optimization procedures. The seen in the comparison of G. riobambae to G. most distant lineages are used to root the tree. nicefori; Scanlan et al. (1980) reported an ID of This method has been determined to be appro- 6, whereas herein we report an ID of 17 and priate for albumin MC'F data in which the large an average of 19 ID for the reciprocal compar- number (580) of amino acid positions in albu- isons. The G. nicefori used in 1980 (KU 18 107 1) mins permits the assumption that there are few was from La Delicia, in the Cordillera Oriental parallel and back-mutation contaminations in of extreme western Venezuela. whereas those the data (Maxson, 1984; Maxson and Maxson, used in the present study (Appendix 1) come 1986). from the Cordillera Oriental and Cordillera Central of southern Colombia, some 400 and 700 km, respectively, from the Venezuelan lo- cality.
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