Anura

Hochstetter’s frog Leiopelma hochstetteri, copyright David M. Green.

Belongs within: Lepospondyli.
Contains: Alytoidea, Pipoidea, Pelobatoidea, Neobatrachia.

The Anura, frogs and toads, are a diverse group of terrestrial to aquatic vertebrates that lack an external tail at maturity and are often adapted for a hopping mode of locomotion. Larvae, if present, are aquatic and legless with a strong, finned tail.

Relict frog sex
Published 6 September 2007
Leiopelma archeyi, from Bruce Waldman.

At least one piece of genetics that almost everyone is familiar with is how our sex is determined—that women possess two X chromosomes while men produce an X and a Y chromosome. What may not be so familiar to most people is that this system is far from universal. Different animals exhibit a wide range of methods of sex determination, both genetic (like our own system) and environmental (such as temperature in crocodiles). In Hymenoptera (ants, bees and wasps) unfertilised eggs produce haploid males, while fertilised eggs produce diploid females. In birds, it is the females that possess two different forms of sex chromosomes (referred to as W and Z), while the male possesses two Z chromosomes. But perhaps the oddest little tale of sex determination involves the strange relictual frog genus Leiopelma.

Leiopelma is a small genus of four living species of frog restricted to New Zealand (a further three species are known from sub-fossil remains—Bell et al. 1998). They represent a basal grade of frogs of which the only other member is the “tailed frog” Ascaphus truei from western North America (different studies disagree as to whether Leiopelma and Ascaphus form the sister clade to or are paraphyletic to all other living frogs—Green & Cannatella 1993; Hay et al. 1995). Leiopelma and Ascaphus retain a number of primitive features that have been lost in other frogs, such nine vertebrae in front of the sacrum and tail-wagging muscles (though the ‘tail’ of male Ascaphus is actually the copulatory organ). Leiopelma also lack a tadpole stage in their life-cycle, hatching straight out into froglets.

The really remarkable thing about Leiopelma, though, is that of the four species living today, at least three have different methods of sex determination from each other. And within two of those species, there are even different populations that differ in their mode of sex determination!

The most primitive state is perhaps that shown by Leiopelma archeyi, in which most populations don’t have distinguishable sex chromosomes. This is the condition in most amphibians, though it has been shown that even in taxa that don’t have heteromorphic chromosomes, sex is still determined genetically (Hayes 1998). However, a heteromorphic W sex chromosome has been recorded in one population of L. archeyi from Whareorino in the King Country (Green 2002). In other features (including genetic features) the Whareorino L. archeyi are almost indistinguishable from Coromandel populations that lack the W chromosome.

The Whareorino Leiopelma archeyi are therefore more like L. pakeka in sex differentiation. Leiopelma pakeka also has a female-ZW/male-ZZ set-up (Green 1988)*. There is only a single population of L. pakeka, restricted to Maud Island, which diesn’t give much scope for variation.

*The species Leiopelma pakeka was recognised only recently (Bell et al. 1998). Previously it had been regarded as a population of the genetically distinct but morphologically almost identical L. hamiltoni, and its genetic structure was described under the latter name. Leiopelma hamiltoni proper is uber-rare, with a population of less than 300 individuals restricted to less than one hectare of habitat on Stephens Island, and does not seem to have yet been investigated for sex chromosomes.

The ultimate wierdness, however, comes when we look at Leiopelma hochstetteri. Most populations of L. hochstetteri have a single sex chromosome in females, while males lack a sex chromosome. This female-0W/male-00 system is unique—no other animal has it. Not one. In fact, it’s so bizarre that not even all L. hochstetteri have it—females of the population on Great Barrier Island lack the lonely W chromosome, and like Coromandel L. archeyi this population does not have morphologically distinct sex chromosomes (Green 1994). The Great Barrier population also lacks the non-sex-related supernumerary chromosomes (or “B” chromosomes) found in other populations (Green et al. 1993). B chromosomes are small, seemingly dispensable chromosomes that are found in a broad scattering of taxa. In species where they are found, numbers of B chromosomes can vary significantly within and between populations, probably because their lack of significant function means a lack of selective control on their propagation. This variation is also seen in L. hochstetteri, where up to 15 B chromosomes were found in individuals of five different populations. The variation in chromosomes between populations is shown below in a figure from Green (1994).

So how did all this come about? I am not aware of any other group of closely-related organisms showing this much variation in so few species. However, it is possible to imagine ZW chromosomes evolving through differentiation of morphologically indistinct sex-determining chromosomes, and this is what appears to have occurred in Leiopelma pakeka and Whareorino L. archeyi. Leiopelma hamiltoni appears to be more closely related to L. archeyi than L. pakeka (Bell et al. 1998), so it would be very interesting to know whether or not it has distinct sex chromosomes.

As for Leiopelma hochstetteri, the sister taxon to all other Leiopelma, phylogenetic analysis of chromosome characters shows that the Great Barrier population, without the extra W chromosome, is probably sister to all other populations. Green et al. (1993) suggest that the 0W/00 system could evolved from a ZW/ZZ system. Either the Z chromosome may have been lost, or (as the authors of the latter study think more likely) it could have been duplicated, giving a ZZW/ZZ pattern that would be karyotypically indistinguishable from 0W/00.

Systematics of Anura

Synapomorphies (from Frost et al. 2006): Prefrontal bone absent; prearticular bone absent; palatine absent; nine or fewer vertebrae; atlas with a single centrum; first spinal nerve exiting from spinal nerve canal via intervertebral foramen; caudal vertebral segments fused into urostyle; hindlimbs significantly longer than forelimbs, including elongation of ankle bones; radius and ulna, tibia and fibula fused; hyobranchial elements fused into hyoid plate; keratinous jaw sheaths and keratodonts present on larval mouthparts; larva with single median spiracle; skin with large subcutaneous lymph spaces; two m. protractor lentis attached to lens.

<==Anura (see below for synonymy)
|--Bombinanura [Archaeobatrachia, Discoglossanura, Lalagobatrachia, Mesobatrachia, Ranoidei, Sokolanura]FG06
| |--AlytoideaFB17
| `--PipanuraFB17
| |--PipoideaPW11
| `--AcosmanuraFG06
| | i. s.: Eurycephalella alcinaeFB17
| |--PelobatoideaEJK08
| `--NeobatrachiaPW11
`--LeiopelmatoideaFB17
|--Ascaphus Stejneger 1899FG06 [AscaphidaePW11]
| |--A. montanusFG06
| `--A. trueiFG06
`--Leiopelmatidae [Amphicoela, Liopelmatina]FG06
|--Vieraella herbstii Reig 1961G88, M93
|--Notobatrachus degiustoi Reig 1955G88, M93
`--Leiopelma Fitzinger 1861 [=Liopelma Günther 1869]FG06
| i. s.: L. waitomoensis Worthy 1987WH02
|--+--L. auroraensis Worthy 1987WH02
| |--L. hochstetteri Fitzinger 1861WH02
| `--L. markhami Worthy 1987WH02
`--+--L. pakeka Bell, Daugherty & Hay 1998BDH98
`--+--L. archeyi Turbott 1942BDH98, WH02
`--L. hamiltoni McCulloch 1919BDH98

Anura incertae sedis:
PhractopsF13
|--P. brevipalmatusF13
`--P. brevipesF13
Callula baleataM89
Notodelphys oviferaH04
LiaobatrachusFB17
|--L. grabauiZBH03
`--L. zhaoiFB17
Enneabatrachus hechtiR00
Eobatrachus agilis Marsh 1887 (n. d.)R00
Comobatrachus aenigmatis Hecht & Estes 1960 (n. d.)R00
Paradiscoglossus americanus Estes & Sanchíz 1982R00
Theatonius lancensis Fox 1976R00
GobiatidaeR00
|--Gobiatoides parvus Roček & Nessov 1993R00
`--Gobiates Špinar & Tatarinov 1986R00
|--G. asiaticus Roček & Nessov 1993R00
|--G. bogatchovi Roček & Nessov 1993R00
|--G. dzhyrakudukensis Roček & Nessov 1993R00
|--G. fritschi Roček & Nessov 1993R00
|--G. furcatus Roček & Nessov 1993R00
|--G. kermeentsavi Špinar & Tatarinov 1986R00
|--G. kizylkumensis Roček & Nessov 1993R00
|--G. leptocolaptus (Borsuk-Białynicka 1978)R00
|--G. sosedkoi (Nessov 1981) [=Eopelobates sosedkoi]R00
|--G. spinari Roček & Nessov 1993R00
`--G. tatarinovi Roček & Nessov 1993R00
Altanulia alifanovi Gubin 1993R00
Palaeophrynos gessneri Tschudi 1839RR00
BatrachusRR00
|--B. lacustris Pomel 1853RR00
|--B. lemanensis Pomel 1853RR00
`--B. naiadum Pomel 1853RR00
Lutetiobatrachus gracilisRR00
Liventsovkia jucundaRR00
Ranavus scarabelliiRR00

Anura [Acaudata, Anoura, Anuri, Anuria, Discoglossoidei, Ecaudata, Ecaudati, Heteromorpha, Leiopelmatanura, Miura, Pygomolgaei, Raniformia]

*Type species of generic name indicated

References

[BDH98] Bell, B. D., C. H. Daugherty & J. M. Hay. 1998. Leiopelma pakeka, n. sp. (Anura: Leiopelmatidae), a cryptic species of frog from Maud Island, New Zealand, and a reassessment of the conservation status of L. hamiltoni from Stephens Island. Journal of the Royal Society of New Zealand 28 (1): 39–54.

[EJK08] Evans, S. E., M. E. H. Jones & D. W. Krause. 2008. A giant frog with South American affinities from the Late Cretaceous of Madagascar. Proceedings of the National Academy of Sciences of the USA 105 (8): 2951–2956.

[FB17] Feng, Y.-J., D. C. Blackburn, D. Liang, D. M. Hillis, D. B. Wake, D. C. Cannatella & P. Zhang. 2017. Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous–Paleogene boundary. Proceedings of the National Academy of Sciences of the USA 114 (29): E5864–E5870.

[FG06] Frost, D. R., T. Grant, J. Faivovich, R. H. Bain, A. Haas, C. F. B. Haddad, R. O. de Sá, A. Channing, M. Wilkinson, S. C. Donnellan, C. J. Raxworthy, J. A. Campbell, B. L. Blotto, P. Moler, R. C. Drewes, R. A. Nussbaum, J. D. Lynch, D. M. Green & W. C. Wheeler. 2006. The amphibian tree of life. Bulletin of the American Museum of Natural History 297: 1–370.

[F13] Fry, D. B. 1913. On a Varanus and a frog from Burnett River, Queensland, and a revision of the variations in Limnodynastes dorsalis, Gray. Records of the Australian Museum 10 (2): 17–34, pls 1–3.

[G88] Gray, J. 1988. Evolution of the freshwater ecosystem: the fossil record. Palaeogeography, Palaeoclimatology, Palaeoecology 62: 1–214.

Green, D. M. 1988. Heteromorphic sex chromosomes in the rare and primitive frog Leiopelma hamiltoni from New Zealand. Journal of Heredity 79 (3): 165–169.

Green, D. M. 1994. Genetic and cytogenetic diversity in Hochstetter’s frog, Leiopelma hochstetteri, and its importance for conservation management. New Zealand Journal of Zoology 21: 417–424.

Green, D. M. 2002. Chromosome polymorphism in Archey’s frog (Leiopelma archeyi) from New Zealand. Copeia 2002 (1): 204–207.

Green, D. M., & D. C. Cannatella. 1993. Phylogenetic significance of the amphicoelous frogs, Ascaphidae and Leiopelmatidae. Ecol. Ethol. Evol. 5: 233–245.

Green, D. M., C. W. Zeyl & T. F. Sharbel. 1993. The evolution of hypervariable sex and supernumerary (B) chromosomes in the relict New Zealand frog, Leiopelma hochstetteri. Journal of Evolutionary Biology 6 (3): 417–441.

[H04] Haeckel, E. 1899–1904. Kunstformen der Natur. Bibliographisches Institut: Leipzig und Wien.

Hay, J. M., I. Ruvinsky, S. B. Hedges & L. R. Maxson. 1995. Phylogenetic relationships of amphibian families inferred from DNA sequences of mitochondrial 12S and 16S ribosomal RNA genes. Molecular Biology and Evolution 12 (5): 928–937.

Hayes, T. B. 1998. Sex determination and primary sex differentiation in amphibians: Genetic and developmental mechanisms. Journal of Experimental Zoology 281 (5): 373–399.

[M93] Milner, A. R. 1993. Amphibian-grade Tetrapoda. In: Benton, M. J. (ed.) The Fossil Record 2 pp. 665–679. Chapman & Hall: London.

[M89] Modigliani, E. 1889. Materiali per la fauna erpetologica dell’isola Nias. Annali del Museo Civico di Storia Naturale di Genova, Serie 2a, 7: 113–124.

[PW11] Pyron, R. A., & J. J. Wiens. 2011. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution 61: 543–583.

[R00] Roček, Z. 2000. Mesozoic anurans. In: Heatwole, H., & R. L. Carroll (eds) Amphibian Biology vol. 4. Palaeontology. The evolutionary history of amphibians pp. 1295–1331. Surrey Beatty & Sons.

[RR00] Roček, Z., & J.-C. Rage 2000. Tertiary Anura of Europe, Africa, Asia, North America, and Australia. In: Heatwole, H., & R. L. Carroll (eds) Amphibian Biology vol. 4. Palaeontology. The evolutionary history of amphibians pp. 1332–1387. Surrey Beatty & Sons.

[WH02] Worthy, T. H., & R. N. Holdaway. 2002. The Lost World of the Moa: Prehistoric life of New Zealand. Indiana University Press: Bloomington (Indiana).

[ZBH03] Zhou, Z., P. M. Barrett & J. Hilton. 2003. An exceptionally preserved Lower Cretaceous ecosystem. Nature 421: 807–814.

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