Tree weta evolution

Tree Weta (Hemideina) Evolution

Chromosome variation
Chromosomes are the parcels of DNA within every cell. Each cell and each individual of a species usually has the same number of chromosomes but the number and size and shape of chromosomes evolves over many generations so that when one compares species one can often observe chromosome differences.

Chromosome rearrangements can cause a reduction in fertility of heterozygotes and thus form a weak barrier to gene flow between populations that have distinct karyotypes. However, many chromosome races remain part of the same species, linked by gene flow across narrow hybrid zones. In Europe the common house mouse (Mus domesticus) has been studied intensively to understand the role of chromosome changes in speciation. Mice have between 40 and 22 chromosomes and the distribution and evolution of the many races of mice have provided an excellent model system for speciation studies. In New Zealand we have few endemic mammals (two rare bat species) but we do have common nocturnal Orthoptera that are proving to be as interesting as mice for their chromosome evolution.

Hemideina thoracica has at least eight distinct karyotypes, found in different part of North Island New Zealand (2n = 11 - 23; Morgan-Richards 1997). Although the numbers of chromosomes vary among races, the DNA content does not, so the variation must involve translocations of both large and small chromosome arms (Morgan-Richards 2005).

Chromosome races of H. thoracica hybridise at their margins with adjacent races, but the extent of resulting gene flow varies among the various combinations (Morgan-Richards & Wallis 2003). Using the width of the hybrid zone at the crater lake of Taupo and the known time since the last volcanic eruption it was possible to estimate the dispersal abilities of these abundant orthoptera; we calculated that these tree weta move at least 100m per generation (Morgan-Richards et al. 2000). Hemideina thoracica has some of the oldest chromosome races found within any single species, anywhere in the world (Morgan-Richards et al. 2001). Using phylogeography we inferred that their chromosome mutations first arose millions of years ago and have since been maintained in spatially separate populations for about five million years. What makes this species unusual is that none of the races has dominated and replaced other races and apparently few races have been lost during climate changes and range contractions of the Pleistocene. Despite this remarkable long history of parapatry the races have failed to speciate – and this makes H. thoracica really exciting and unusual. By comparing the widths of the chromosome hybrid zones one can infer the relative fitness of individuals that are chromosome heterozygotes. We found that hybrid zone widths, and therefore fitness levels, differ by almost two orders of magnitude (0.5 km – 50 km; Morgan-Richards & Wallis 2003). Strangely enough, in this species, the hybrid zones where hybrids suffer the greatest disadvantage are marked by tiny chromosome changes, whilst wide hybrid zones where hybrids suffer much less fitness-disadvantage are marked by large chromosome translocations.

Another tree weta species (Hemideina crassidens) also has intraspecific chromosome variation that includes B chromosomes in one island population. This species is very unusual in that the B chromosomes are only in the males (Morgan-Richards 2000). Hemideina crassidens is also unusual in that the rearrangements that resulted in two of the known chromosome races (2n = 16(XX) 15(XO); 2n= 20(XX) 19(XO)) seem to have arisen from fissions of metacentrics not fusions (Morgan-Richards 2002). Chromosome rearrangements that fuse two acrocentric chromosomes to form one large metacentric chromosome (Robertsonian Translocations) are quite common in mice and shrews and spiders, but fissions of chromosomes have rarely been documented. Captive breeding experiments provided evidence that the rearrangements were simple fission/fusion events and F1 hybrids seemed developmentally normal. Phylogenetic studies with mtDNA sequence data indicate that the 19-chromosome race is probably derived from the 15-chromosome race (Morgan-Richards 2002) via chromosome fissions. In comparison, within H. thoracica chromosomes appear to have generally fused to reduce diploid numbers.

Other species of Hemideina are chromosomally more conservative (Morgan-Richards and Gibbs 2001), but one widespread giant weta (Deinacrida connectens) also has a good deal of karyotype variation with seven distinct karyotypes recorded (2n = 17-21; Morgan-Richards and Gibbs 1996).

DNA phylogeography
The high level of chromosome variation of H. thoracica and H. crassidens is matched by some of the highest levels of intraspecific DNA sequence diversity ever reported. For example, haplotypes in the same population of H. thoracica can differ by as much as 7.6% (uncorrected P distance, 550 bp COI mtDNA), and among populations the maximum distance is 9.5% (Morgan-Richards et al. 2001). This level is common between different species of the same genus of other taxa but unusual within a species, even among invertebrates. Four factors combine to produce these record levels of genetic diversity. First, New Zealand retained forest flora and fauna during the glacial cycles of the Pleistocene and so unlike the extensively studied faunas of Europe and North America, some New Zealand taxa retained populations and their genetic variation throughout this time. Second, H. thoracica populations were isolated on islands during the Pliocene, which we think led to the fixation of novel chromosome races and distinct mtDNA haplotypes. These islands are now connected and gene flow among chromosome races leads to populations that are polymorphic for very different mtDNA haplotypes. Third, the island populations failed to speciate, perhaps due to the weta’s simple mate recognition systems and genetic compatibility. Fourth, the mtDNA of H. thoracica has extraordinary little base bias. Most insect mitochondrial genomes have many more A + T than C + G bases (typically about 70% A + T), in contrast H. thoracica has 58% (A + T). This facilitates a slightly more rapid accumulation of synonymous mutations. Thus we find record levels of genetic diversity within and among populations of tree weta (Hemideina).

The distribution of genetic diversity within H. thoracica owes much to isolation on Pliocene islands and recolonisation following volcanic eruptions. Both recent Taupo eruptions (< 2,000 years ago) and older (> 25,000 ya) Taupo eruptions have had major effects on the distribution of mtDNA haplotype diversity (Morgan-Richards et al 2000; 2001) in the central North island, New Zealand. Further north the phylogeographic pattern reflects the Pliocene archipelago. In contrast the centre of genetic diversity of H. crassidens seems to be between North and South Island. The two major islands of New Zealand were most recently connected 10,000 – 20,000 years ago when H. crassidens populations on each island would have been in contact. Hemideina crassidens is more cold tolerant than the more northern H. thoracica and during the repeated glacial cycles of the Pleistocene the distributions of these two species probably oscillated up and down the country. On the central north island mountains there are populations of H. crassidens entirely surrounded by the lower altitude H. thoracica – relicts of a past more northerly distribution of H. crassidens (Trewick & Morgan-Richards 1995). The isolation of the mountain H. crassidens populations suggests the two species competitively exclude each other, and who wins depends on climate. We plan to study adaptation and mate recognition in these two species to complement our cytogenetic knowledge. In South Island New Zealand the most abundant and widespread of the giant weta (Deinacrida connectens) has populations on most mountain ranges. Phylogeographic structure of the scree weta D. connectens indicated matrilineal isolation since the Pliocene when the mountains formed (Trewick et al. 2000).

With a combination of cytogenetics, phylogeography and natural history I hope to spend the rest of my career uncovering the evolutionary history of New Zealand weta.

References

Morgan-Richards, M. and Gibbs, G. W. 1996. Colour, allozyme and karyotype variation in the New Zealand Giant Scree Weta Deinacrida connectens (Orthoptera: Stenopelmatidae). Hereditas, 125: 265-276.

Morgan-Richards, M. 1997. Intraspecific karyotype variation is not concordant with allozyme variation in the Auckland tree weta of New Zealand, Hemideina thoracica (Orthoptera: Stenopelmatidae). Biological Journal of the Linnean Society, 60: 423-442.

Morgan-Richards, M., Trewick, S. A. and Wallis, G. P. 2000 Characterization of a hybrid zone between two chromosomal races of the weta Hemideina thoracica following a geologically recent volcanic eruption. Heredity, 85(6): 586-592.

Morgan-Richards, M. 2000. Robertsonian translocations and B chromosomes in the Wellington tree weta, Hemideina crassidens (Orthoptera: Anostostomatidae). Hereditas, 132: 49-54.

Morgan-Richards, M. & Gibbs, G. W. 2001. A phylogenetic analysis of New Zealand giant and tree weta (Orthoptera: Anostostomatidae: Deinacrida and Hemideina) using morphology and genetic characters. Invertebrate Taxonomy, 15: 1- 12.

Morgan-Richards, M., Trewick, S. A., and Wallis, G. P. 2001. Chromosome races with Pliocene origins: evidence from mtDNA. Heredity, 86(3): 303-312.

Morgan-Richards, M. 2002. Fission or fusion? Mitochondial DNA phylogenetics of the chromosomal races of Hemideina crassidens (Orthoptera: Anostostomatidae). Cytogenetics & Genome Genetics, 96: 217-222.

Morgan-Richards, M. and Wallis, G. P. 2003. Degree of cytogenetic differentiation fails to predict hybrid zone width in the weta Hemideina thoracica (Orthoptera: Anostostomatidae). Evolution, 57: 849-861.

Morgan-Richards, M. 2005. Chromosome rearrangements are not accompanied by expected genome size change in the tree weta Hemideina thoracica (Orthoptera, Anostostomatidae). Journal of Orthoptera Research 14(2): 143-148.

Trewick, S. A., Wallis, G. P. and Morgan-Richards, M. 2000. Phylogeographic pattern correlates with Pliocene mountain-building in the alpine scree weta (Orthoptera, Anostostomatidae). Molecular Ecology, 9(6): 657-666.

Trewick, S. A., Morgan-Richards, M. 2004. Phylogenetics of New Zealand’s tree, giant and tusked weta (Orthoptera: Anostostomatidae): evidence from mitochondrial DNA. Journal of Orthoptera Research 13(2): 185-196.