Wednesday, December 23, 2015

[Herpetology • 2015] Genetics, Morphology, Advertisement Calls, and Historical Records Distinguish Six New Polyploid Species of African Clawed Frog (Xenopus, Pipidae) from West and Central Africa

Fig 7. Pictures of resurrected and new species in life; Xenopus calcaratusXparafraseriXmellotropicalisX. eysooleX. allofraseriX. kobeli and  X. fischbergi


African clawed frogs, genus Xenopus, are extraordinary among vertebrates in the diversity of their polyploid species and the high number of independent polyploidization events that occurred during their diversification. Here we update current understanding of the evolutionary history of this group and describe six new species from west and central sub-Saharan Africa, including four tetraploids and two dodecaploids. We provide information on molecular variation, morphology, karyotypes, vocalizations, and estimated geographic ranges, which support the distinctiveness of these new species. We resurrect Xenopus calcaratus from synonymy of Xenopus tropicalis and refer populations from Bioko Island and coastal Cameroon (near Mt. Cameroon) to this species. To facilitate comparisons to the new species, we also provide comments on the type specimens, morphology, and distributions of X. epitropicalis, X. tropicalis, and X. fraseri. This includes significantly restricted application of the names X. fraseri and X. epitropicalis, the first of which we argue is known definitively only from type specimens and possibly one other specimen. Inferring the evolutionary histories of these new species allows refinement of species groups within Xenopus and leads to our recognition of two subgenera (Xenopus and Silurana) and three species groups within the subgenus Xenopus (amieti, laevis, and muelleri species groups).

Fig 7. Pictures of resurrected and new species in life; 
Xenopus calcaratusX. parafraseriX. mellotropicalisX. eysooleX. allofraseriX. kobeli and  X. fischbergi

Host-Parasite co-evolution: Influences of allopolyploid evolution

The parasite fauna of Xenopus is characterized by its extraordinary richness. Within metazoan parasites, for instance, there are over 25 genera from 7 major invertebrate groups; a richer assemblage than in most other anurans. This diversity reflects a dual origin of the parasites: some (such as Protopolystoma, Dollfuschella, Oligolecithus and Progonimodiscus) are typical of anurans; others (including Gyrdicotylus, Cephalochlamys and the camallanid nematodes) are typical of fish, representing transfers associated with ecological overlaps in habitat and diet. For both subsets of parasites, the representatives infecting Xenopus have exceptional specializations such as the brood pouch and velum of the leech Marsupiobdella, the attachment organ and excretory system of the monogenean Gyrdicotylus, and the ereynetal organ of the mite, Xenopacarus.

In addition to parallel evolution of host and parasite, patterns of parasite infection are influenced by allopolyploid evolution of Xenopus. For example, species of Cephalochlamys occur in all tetraploid species of subgenus Xenopus so far examined, but not in octoploids, even when the octoploids co-occur with infected X. victorianus [a tetraploid]. This is consistent with the possibility that increased gene dosage or inheritance of resistance genes with complementary functions in octoploids confers parasite resistance. Parasites from the genus Protopolystoma provide a counter-example of increased susceptibility of higher ploidy levels. Most species in this parasite genus infect only one anuran host species. However, the tetraploid species X. victorianus and X. parafraseri and the octoploid species X. wittei each are infected by two Protopolystoma species (X. victorianus: P. xenopodis and P. microsclera; X. parafraseri: P. fissilis and P. ramulosus; X. wittei: P. fissilis and P. simplicis). That P. fissilis occurs in X. parafraseri and in X. wittei could represent shared inheritance of an ancestral susceptibility derived from a diploid ancestor. Interestingly, in X. victorianus and X. wittei, although two parasite species occur side-by-side in the same host populations, they never co-occur as adults within the same host individuals.

The effects of host interspecies hybridization (not involving genome duplication) on susceptibility to parasite infection have been investigated in X. laevis and X. muelleri. These host species each have species-specific Protopolystoma parasites and laboratory-generated F1 hybrids are also largely resistant. This study illustrates a selective advantage of host hybridization for enhanced immune function to helminth parasites that extends to other important pathogens such as viruses and bacteria. This advantage could have facilitated the establishment of newly emerged polyploid species alongside their parental species in the same habitats.

Central Africa: A species diversity hotspot for African clawed frogs

Over half of Xenopus species occur in Central Africa, including the six new species described here, the resurrected species X. calcaratus, and nine other previously known species: X. amieti, X. andrei, X. boumbaensis, X. epitropicalis, X. fraseri, X. longipes, X. poweri, X. pygmaeus, X. tropicalis. This list includes representatives of both subgenera, and each species group as newly defined (but not the Ethiopian endemic X. largeni). Three of these species (X. epitropicalis, X. poweri, and X. pygmaeus) have distributions centered in the Congo Basin, X. fischbergi has a large range over much of the northern Congo Basin, but the rest are probably endemic to the portion of Central Africa northwest of the Congo River.

What could explain this high species diversity in Central Africa? Persistent forest habitat could have played a role in maintaining or augmenting species diversity of African clawed frog. Indeed, the Albertine Rift region also hosts a high species diversity of African clawed frogs, including several octoploids (four species) and a dodecaploid, and this region probably harbored forest habitat for an extended period. Another feature of the Central African Xenopus diversity is a large number of species with high ploidy levels; specifically three of the seven octoploid species and three of the four described dodecaploid species occur in Central Africa. These species are a result of multiple independent allopolyploidization events that combined a few ancestral genomes in several unique ways. The diversity of octoploid and dodecaploid species raises the question of whether allopolyploidization conferred a selective advantage for species in Central Africa, such as those related to immune function discussed above.

Ben J. Evans, Timothy F. Carter, Eli Greenbaum, Václav Gvoždík, Darcy B. Kelley, Patrick J. McLaughlin, Olivier S. G. Pauwels, Daniel M. Portik, Edward L. Stanley, Richard C. Tinsley, Martha L. Tobias and David C. Blackburn. 2015. Genetics, Morphology, Advertisement Calls, and Historical Records Distinguish Six New Polyploid Species of African Clawed Frog (Xenopus, Pipidae) from West and Central Africa. PLoS ONE. 10(12): e0142823  DOI:  10.1371/journal.pone.0142823

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