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Neo-XY Sex Chromosome Mechanisms in Two Species of Tettigonioidea (Orthoptera)1

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Neo-XY Sex Chromosome Mechanisms in Two Species of Tettigonioidea (Orthoptera)1 190 Neo-XY Sex Chromosome Mechanisms in Two Species of Tettigonioidea (Orthoptera)1 M. J. D. White, Alejo Mesa and R. Mesa Department of Genetics, University of Melbourne, Australia, and Laboratorio de Biologia de Insectos, Facultad de Agronomia de Montevideo Received June 7, 1966 Introduction Studies of the sex chromosome mechanisms of the short-horned grasshoppers (Acridoidea) have demonstrated the existence of numerous species in which the original XO:XX mechanism has been replaced by an XY:XX one, as a result of a centric fusion between the original X and an acrocentric autosome (White 1940, King 1950, Mesa and Mesa 1966, White and Cheney 1966). By contrast, about a hundred species of long-horned grasshoppers (Tettigonioidea) that have been investigated have almost all been found to have XO males (Asana, Makino and Niiyama 1938, White 1941b, Hareyama 1941, Piza 1945, 1950 a, b, 1954, 1958). Newly-arisen XY mechanisms are of considerable genetic interest for several reasons. We may expect to find in them a series of genetic transformations, involving evolutionary hetero chromatinization of chromosome regions, the acquisition of new "differential" segments and, perhaps, the development of new mechanisms of dosage compensation. The indications are that in the Acridoidea not one of the numerous neo-XY systems that have arisen has proved a long-term evolutionary success. Thus they tend to occur in isolated species or small groups of closely related species, and there is not even a single moderately large genus in which all the members have neo-XY sex chromosome mechanisms. The X1X2Y:X1X1X2X2 systems that have been described in a few Acridoidea (King and Beams 1953, White 1953, Mesa 1962, 1963, White and Cheney 1966, Mesa and Mesa 1967) represent a further stage in the development of the sex chromosome mechanism, and have arisen by an additional Y-autosome fusion. They likewise seem to be short-lived failures in an evolu tionary sense. On the other hand, the well-known X1X2Y mechanism in one section of the Praying Mantids (order Mantodea) has arisen in a different manner, by a mutual translocation in an XO form (i.e. without passing through a neo-XY stage); it occurs throughout a whole group of large genera and must be regarded as having been a conspicuous evolutionary success (White 1940, 1941a, 1965; Hughes-Schrader 1950, 1953). To date, only three species of Tettigonioidea that deviate from the usual XO mechanism in the male seem to have been recorded. The first is the well-known North American "Mormon Cricket" An abrus simplex (Decticinae), for which the only information is the very old and unsatisfactory account of McClung (1902 , 1905, 1914) from which one can conclude that a neo-XY mechanism is probably present in this species , the chromosome number being 2n•‰= 32 or 34, rather than 33, as stated by McClung. The others are an unidentified species of Isopsera (Phaneropterinae) with XY males and Letana atomifera (Tettigoniinae) with X1X2Y males, both from India (Dave 1965). In the present paper we report two more species of Tettigonioidea with neo-XY mechanisms, Theudoria melanocnemis (Stal) (Phaneropterinae) from South America and Yorkiella pieta Carl (Listroscelinae) from Australia. 1 Supported in part by Public Health Service grant GM 07212 from the Division of General Medical Sciences, U. S. National Institutes of Health and in part by a Grant from the Rothmans University Endowment fund. 1967 Neo-XY Sex Chromosome Mechanisms in Tettigonioidea 191 Material and methods In the case of Theudoria the testes of 15 specimens were fixed in acetic alcohol (1:3) and squashes prepared, after Feulgen staining. The material was collected at the following localities: Brazil: 3_??_, Rio Grande do Sul, Pelotas, 8. II. 64; 1_??_,Rio Grande do Sul, 54km. N. of Pelotas 11. II. 64; 4_??_, Rio Grande do Sul, Lagoa Vermelha, 18. II. 64; 1_??_,Rio Grande do Sul, Samanduva, 18. II. 64; 1_??_,Rio Grande do Sul, Trinidade, 22. II. 64; 1_??_,Rio Grande do Sul, Vacarias, 26. II. 64; 1_??_Rio Grande do Sul, 33km. N. of Passo Fundo, 25. II. 64; Uruguay: 1_??_,San Jose, Santa Lucia, 1. V. 63, Argentina: 2_??_, Misiones, Bernardo de Irigoyen, 16. III. 65. The material of Yorkiella picta consisted of three males, one from 5 miles SW of Whyalla, Eyre Peninsula, one from 9 miles WNW of Monia Gap, New South Wales, and one from 16 miles N of Alice Springs, Northern Territory. In addition, a male of another species of Yorkiella ("species 1" in the Australian National Insect. Collection) from 6 miles SW of Warwick, Queensland, was studied. The material was sectioned and stained in crystal violet. Three species of this genus are known to exist (pitta, sp. 1 and sp. 2); they are large insects which occur in areas where the shrub stratum of the vegetation is well developed, but are distinctly uncommon. Observations 1) Theudoria melanocnemis Spermatogonial metaphases show 30 chromosomes, one of these being metacentric, the others acrocentric. In the primary spermatocytes 14 autosomal bivalents are formed. They can be grouped according to length into 5 long bivalents, 2 medium sized ones and 7 small ones (Fig. 1). All of them appear to Fig. 1. T. melanocnemis. First metaphase chromosomes arranged in order of size. Sex chromosomes at the right hand end (note precociousseparation of the X and Y). be euchromatic in the prophases of the first meiotic division. The sex mechanism is of the neo-XY type, the X being a metacentric and the largest element in the karyotype. Its arms are unequal in length, the long arm measuring about twice the length of the short one. The Y chromosome is a large acrocentric element, its length being about the same as that of the longer limb of the X. During the prophase of the first meiotic division, the whole of the sex bivalent appears heteropycnotic, especially the unpaired longer arm of the X which has a constric tion near its distal end (Fig. 2). This constriction is not visible at other stages of 192 M. J. D . White, A. Mesa and R. Mesa Cytologia 32 Fig.2. T. mel anocnemis. Some diplo tene bivalents in a squash preparation, including two sex bivalents. The autosomes are euchro matic and the sex chrom somes hetero chromatic. Fig. 3. T. melanocnemis. First metap hase from an individual collected in Bernardo de Irigoyen (Arg entina), with a supernu merary chromsome (S). 1967 Neo-XY Sex Chromosome Mechanisms in Tettigonioiidea, 193 Figs. 4-7. 4, T. melanocnemis. First anaphase. 5, T. melanocnennis. A first metaphase showing asynapsis of the sex chromosomes. 6, T. melanocnemis. First metaphase of an individual from Pelotas (Brazil) with the large supernumerary chromosome towards the same pole as the Y. 7, T. melanocnemis. Similar to Fig 6, but with the supernumerary directed towards the same pole as the X. 104 M. J. D. White, A. Mesa and R. Mesa Cytologia 32 meiosis. The short arm of the X-chromosome is associated with the Y by a term inal chiasma. The latter chromosome appears to be bent in half during first prophase, so that it is difficult to study its morphology. In first metaphase the small and medium sized bivalents show one chiasma and the large ones one or two chiasmata each. The neo-X and neo-Y chromosomes begin their anaphase separation earlier than the autosomes (Figs. 1, 3) and in a few nuclei the sex chromosomes were asynaptic (Fig. 5). One individual collected in Bernardo de Irigoyen (Argentina) showed a super numerary chromosome in some nuclei (Fig. 3). Another individual collected in Pelotas (Brazil) showed a large supernumerary chromosome. In 13 first metaphases observed, this element was orientated on the same side of the equator to the Y in 10 cells (Fig. 6) while in 3 cells it was on the same side as the X (Fig. 7). 2) Yorkiella picta This is likewise a neo-XY species, but the details of the mechanism are very different. 2n•‰ =20, the neo X being a huge metacentric with unequal arms (Fig. 8a). The neo-Y is a medium-sized acrocentric which cannot be distingui shed with certainty from several of the medium-sized autosomes. At diplo tene it can be clearly seen that the long limb of the X is the only heteropycnotic element in the Fig. 8. Yorkiella picta. a, spermatogonial metaphase (identification nucleus (Fig. of the neo-Y chromosome not certain). b, diplotene. c, first metaphase 8b). At this in polar view. d, the same in side view. e, the two kinds of second stage the metaphase. heteropycnotic 1967 Neo-XY Sex Chromosome Mechanisms in Tettigonioidea 195 limb of the X often shows some degree of relic coiling . The shorter euchromatic arm of the X is associated with the euchromatic Y , of similar length, usually by means of two chiasmata, one of which at least is interstitial . There can be very little doubt that the whole, or almost the whole of the neo-Y is homologous to the entire short arm of the neo-X. At first metaphase the sex bivalent is a very conspicuous structure, with the very long free arm of the X lying more or less "horizontal" , the Y and the pairing arm of the X being "vertical" (Fig . 8c, d). There is usually a clear indication of the presence of more than one chiasma in the sex bivalent. The neo-X and the neo-Y do not disjoin precociously in Yorkiella pieta as they do in Theudoria and in Isopsera (Dave 1965). The second meiotic division (Fig. 8e) are naturally ofs two easily distinguishable types, according to whether Fig.
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