Relict Frog Sex

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 (and one I only discovered recently) involves the strange relictual frog genus Leiopelma (the species Leiopelma archeyi is shown in a photo from the page of Dr. Bruce Waldman).

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.

REFERENCES

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.

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.

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.