MULTIPLE SEX- MECHANISMS AND IN

BY ELISABETK GOLDSCHMIDT Department of Zoology, The Hebrew University, Jerusalem, Israel (With Two Text-figures) Received ~'n July 1949 Almost twenty-five years have passed since Muller (1925) pointed ou~ why polyploidy must be rare in bisexual animMs. He assumed tha~ two tetraploids of different sex were most unlikely to appear simultaneously in one population and to breed together. 'If, however, by a rare coincidence two or more tetraploids of different sex have beeu formed and they breed together, the problem of an efficient isolation would arise. In XXYY individuals there would be more tendencies for like to synapse with the like (XX, Y Y) than with the unlike homologue (X Y). There would thus be a tendency for the formation of X Y- '--and this would involve a breMcdown o f the mechanism of sex determination. --' The only way in which the tetraploid might be freed from the above reproductive handicap would be through the fusion of like sex- into single masses of double size and "potency" or through the formation of some temporary attachment or attraetiou between them operative at the reduction division in such a manner as to carry like chromosomes to the same pole.' This argument has been quite generMly accepted, and it is assumed, accordingly, that polyploidy has played its part, mainly or exclusively, in such groups of animals, in which parthenogenetic or hermaphroditic (White, 19~0b) is either facultative or obligatory. Classical instances of polyploidy coupled with are known in Artemia saline (A~'tom, 1928; Gross, 1932; Barigozzi, 1934, 1946), Psychidae (Seller, 1923, 1927, 19~i8) and in terrestriM Isopods (Vandel, 1928, 193~, 1940, 1947). More recently the cases of the Curculionidae (SuomMMnen, 19~i0, 1947, 19~8) and of the Tettigonid Saga (Matthey, 19~11, ] 94:6; Goldschmidt, 194-6) have been added to this series. After a very thorough review of closely related with widely different chromosome numbers, White (19~i5) concludes that one should be eareN1 about accepting any clMms that polyploidy has played a role in the of animals: 'The evidence has never been of a concNsive kind.' The case for polyploidy in the earwigs, a group apparently devoid of parthenogenetic tendencies,, has recently beml expounded by Bauer (19~7). He shows that the knowu chromosome numbers in this group easily arrange themselves in two series : a lower (diploid) series with 2~ = ] 2-14- and a higher (tetraploid) series with 2n = 2~-25. In the latter series four out of five of the species investigated possess a multiple sex-chromosome mechanism (X1X2Y) in some or all of their members. Bauer concludes that the evolution of the multiple sex-chromosome mechanism must be connected with polyploidy. This conclusion is espeeiMly convincing since he himself describes a hexaploid species, Prolabi~ araohidis, possessing three X-chromosomes and a Y. The tetraploid series can now be increased by another member, Fo~Jicula s,m,y,rnensis Serv. Observations are based on two tomes. One of these was fixed in modified Bouin ELISAB ETI-[ GOLD SCI-[IVIIDT 635 (picrie acid sat. 15 c.c., formalin 5 c.e., glacial acetic ~ c.c.), the other in strong Flemming. The chromosome number is 2n=2l, i.e. somewhat lower than in the other tetraploid species; the sex-trivalent is triangular or chain-like on the [~rst metaphase spiudle. Second mctaphase plates contain either ten or eleven members (of. Fig. t). The known data on the cytology of Forficulina are summarized in Table 1.

Table 1. ~orfic'ulina Chromosome Sex- no. of chromosome Species rome (2n) complement Author Labidura bidens 12 X Y Morgan, 1928 L. rl/paria 14 XY Asana & l~'[alr 1934 Labia minor 14 XY Morgan, 1928 Anisolabis maritime 25, (24) XiX2Y Kornh~mser, 1921; 5iorgan, 1928; (gandolph, 1908) A. marginalis 25 X1X.Y Sugiyama, 1933 A. armadillos 25 XtXeY hiorg,~n, 1928 7~'o~:ficula smyrncnsis 21 X1X 2 Y Aut,hor, unpublished 1~~. auricularia 24 XY SLovens, 1910; l?ayne, 1914; l~'Iorgan, 1928; Callan, 1941 25 XiXoY l?ayne, 1914; BioNan, 1928; CMlan, 1941 F. scudderi 24 XY Misra, 1937 Al~lerygida albi~ennis 24 X Y Bauer, 1947 Prolabia arachidis 38 XiXeX~Y Bauer, 1947

Bauer assumes that in an allopolyploid a' fnsion' of the two Y-ehronmsomes (transloca- tion of a large section of one Y to the other) would be sufficient to ensure normal segregation of the two X-chromosomes to the same pole. However, the possibility of autotetraploidy cannot be completely dismissed, especially since the nmnber of ehiasmata is low in earwigs (of. Callan, 1961). This would tend to facilitate a + normal reduction in polyploids of either type.* An X~X~Y mechanism might arise in either an auto- or an allopotyploid as the conse- quence of a single paracentrie inversion in one of the two X-chromosomes in the region over which X and Y are homologous (of. Fig. 2). In the tetraploid male germ-line X- and Y-chromosomes, respectively, will tend to pair prevalently among t~hemselves (Fig. 2b). If one of the X-chromosomes contains a paracentric inversion in the Y-homologous region, synapsis between the two X-chromosomes will occur by loop formation. Crossing-over in this region may occur repeatedly in the same testis and will give rise in each case to a dicentric eN~omosome and an aeentric ll'agment (Fig. 2@ The bridges formed by the will break in various manners in the subsequent divisions (eft McClintock, 1961), and after 'healing' of tee ends a whole variety of X-chromosolnes will have arisen containing different portions of the Y-homologous region, but each with a full sex-determiNing set. In the subsequent generations selection will preserve two of these X-fragments containing complementary portions of the Y-homologous region. In the presence of a trivMent consisting of a Y- and two X-chromosomes the second Y will fail to find a partner and will be lost (Fig. 2d). It should be nbted that all the changes involved occur as the direct result of a single inversion and that inversions are among the most frequent types of chromosome aberrations. Unfortunately, the sex-trivalent in Forfieulids, when it first becomes conspicuous, is

* Mickcy (1945) describes completely normal synapsis and disjuncLion wibhouL format,ion of mulLivalents in the polyploid germ cells of the insec~ Romalea microptera. f 6 \

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o. ELISAm~TI-~ GOI~DSCI-I~IIDT ~37 already fully condensed, and its mode of prophase pairing cannot, therefore, serve to test either of these theories (cf. Callan, 19,14). It is interesting to note that F. au~'icula,ria is about to normalize its ,sex-determiniag mechanism and that a sex-determining region of double strength must be contMned in the single X of the 24-type tomes of this species, In Y. scudde'ri and in Al)lerygida alb@ennis the process of normMizatim~ appears to be complete.

Homologou~ regioll ~*"

a /) c d e f g

Sex-determining I eglon abcdefg x/ (~) @

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Fig. 2. Kypotha~ieal evolution of scx-trivalent. (a) X aud Y in the diploid. (h) X attd Y itt {,he hegraploid, (o) Lvol) ibrmation as the result 6f ~ l~araeentric inversion hi one X, Crossing-over giv:mg rise to dieentrie bridge and aeengrie fi'agment, (d) Y-eln'omosome pairh~g with two products of breakage resNting ii'om the bridge (X 1 a~d X,).

It seems legitimate to inq~fire whether in other groups, too, the occurrence of a multiple sex-chromosome mechanism might furnish a circumstantial evidence for poiyploidy. The case is very clear in tim genus Gry~ota,ITa (cf. Table 2).

Table 2. Gryllotalpa Chromosome Sex- no- of chromosome Species mMe (2n) complement Author G. gryllolalTa 12 (W. Europe) XY Payne, 1916 ; Barigozzi, 1933 ; de Whfiwar~er, t927, 1937 14 (Roum~lfia) X Y S~copoe, 1939 15 (S. Italy) XO do Winiwarter, 1927, 1937; l~arigozzi, 1933 19, 23 XO Kushnh', 1948, 1952 23 XO Ohmaehi, 1929; Asana, 1Kaldno & Niiyama, 1940 G. borealis 23 X1X~ Y P.aync, 1916

G, bqrecdis (PayE% 1916) has [m~g been knowr, to l~ossess a~ peculiar type of segregation, an accessory chronlosome (apparently X,) passing invariably to the same pole as the X (apparently X1). On the other hand, G. c~'~'ieancbwith the same chromosome number (2n=23) possesses a normal sex-determining mechanism (XO), but the X-chromosome is excessively large. A much lower chromosome number is found in G. 9ryllotcdpa, which in 4:38 Mult@le sex-chromosome mechanisms and polyploidy in animals western Europe has only 12 chromosomes, while higher numbers occur farther east, and south. The sex mechanism is XO or XY, but the X is always one of the mediuul-sized chromosomes, l~ecently, Kushnir (19,f8, 1952) has poiated out that polyploidy must have occurred in the evolution of the genus. He furnishes conclusive evidence that 2n = 12 must be the primitive nmnber of the group. He shows that the chromosome variation within

Table 3. Pentatom,idae Chromosome Sex- no. of ehronlosomo Species male (2n) eomplenmnb Aut,hor l~enlatoma sen,ills 6 X Y Wilson, 1913 Oebalus pugnax 10 X Y Wilson, 1909 E'uschist.us crassus 12 X Y li'oog & S~robell, 1912 E'uscMstus 4 spp. 14 XY Wilson, 1906 Coen,'u,s delius 14 X Y Mont,gomew, 1906 Euryden~a rugosa 14 X Y Nashimnra., 1927 Mormidea, lugens 14 X Y Montgomery, 1906 Nezara, hilaris, virid'ula 14 ~gl" Wilson, 1905, 1911 Peribal'us limbolaris 14 X Y Men,gerainT, ] 906 Perillus co~/lue'ns 14 X Y Montgomery, 1906 Podisus 2 spp. 14 X3 ~ Wilson, 1909 Podis'us 3 spp. 16 X Y Montgomery, 1906 ; Wilson, 1909 Cosmopepla, carmlfex 16 X Y Montgomery, 1906 ".l'richopepla semivitlata 16 X Y Montgomery, 1900 Ba,nasa dimidiala, 16 X Y Wilson, 1907 B. cal'va 26 ? Wilson, 1905 Thya.nta cuslator 10 XY Wilson, 19 ll Thyanta calceala 27 XaX,,Y Wilson, 19ll

the species G. gryllot@pa is due to the addition of heteroehrolnatie polysomics, while in the other two species the number 2n = 23 was reached by doubling of the original 12. Thus, the tetraploids of dryllotalpa exhibit both mechanisms which, according to )~[uller, may eliminate the 'reproductive handicap' of polyploids. In G. borealis two X-chromosomes segregate to the same pole, wNle in G. @'icana two X's have fused into a single larger mass. Table 3 shows that in the Pentatomidae, too, the multiple sex mechanism of fhyant~ calceata (2n=27) is accompanied by tetraploidy, since the majority of the investigated species of the faanily have 2n = 14 + 2, which, in its turn, may be a multiple of a lower primitive number (eft Pentatoma senilis, 2'n = 6). The case of the Mantida.e (of. Table 4) is by far more complicated. Here the multiple sex n~echanism is restricted to species with the chromosolnc number 2n=27, with the

Table 4. Mantida,e Chromosome Sex- no. of ehrolnosonm Species male (2n) eomplemen~ Aut,hor Acontiolhespis sp. 15 XO White, 1941 Miomantis sp. 15 XO White, 1941 Callimantis antillarum 17 X O White, 1938 Paratenodera sbnensis 27 X, X 2 Y Whil~e, 1941 fl'enodera ari&ifolia 27 X1X.~ Y Whil, c, 1941 Sphodromantis sp. 27 XlX 2y White, 1941 S. vlridis 23 X1X=Y Whi~c, 1941 dl'[a'nlis rcligiosa, 27 X1XuY King, 1931 Hierodula, sp. 27 .krlX2 Y Asa.na, 1934 s carolina 27 XIX~Y King, 1931 Choeradodis rhombicollis 3 l X1X 2 ]7 1-1ughos-Schrader, 1943 Ameles abjecta 29 XO White, 1941 Empusa, ege.na, 27 2~O WhiLe, 1941 Gongylus gongyloides 27 XO White, 1941 Iris oraloria 25 XO Whil, e, 194 l ELISABETI{ GOLD SC2I-IIVIIDT 439 exception of Choe~'adodis rhombicoIlis (2n = 3[) and of SIJhod'romantis vb'idis (2n = 23). The nmnber 27 is, however, present in another species of the genus ~S'phodrom.antis. Much lower ehronmsome numbers, i.e. 2n = 15 and 2n = ]7, are also found in members of this group. White (1940 a,, 194-] ) proposes that the multiple sex mechan ism of the XIX 2 Y species may have arisen in an ancestor by exchange of arms between the X-chromosome and one nmmber of an pair. He does not consider the possibility of tetraploidy. Still, it is by no me-ms clear why such a translocation, if it did once arise, should have been perpetuated in nmnerous species of Manteinae, since the new sex-chromosome mechanism involves a considerable risk of non-disjunction, while conferring no obvious advantage upon the species. On the other hand, if the nmltiple mechanism arose simultaneously with the establishment of polyploidy, the advantages accruing fi'om the latter may well com- pensate for the loss of gametes entailed by the former. It should not be overlooked that among the species of lVlantids combining a high chromosome munber with an XO mechanism, there are some possessing an excessively large X-cln'omosome (Ameles abjecta,, E'm,~ousa egena, Gongylus gongyloides). These large X-chromosomes may have arisen, as in Oryllotalpa e~/'ricana, by fusion of two normal-sized elements. It might be conceived that not every spindle mechanism is adapted to carry such cumbersome chronmsomes in a set otherwise consisting of much smaller elements. And this may furnish the explanation for the remarkable persistence of the X1X~Y mechanism throughout the Manteinae. While the Pleeoptera may possibly constitute an additional instance, there are many cases of multiple sex mechanisms among animals which do not lend themselves to a similar interpretation. Thus Paratylotropidia with an X~X~ Y mechanism has the character- istic eln'omosonre nmnber of Acridiidae in general. In Cimex the large fluctuation in the number of X-chromosomes (2-15) indicates that they are heterochromatie supernmneraries comparable to the B-chromosomes of . Nor do the known chromosome nmnbers in Araneida warrant a hypothe,~is based on polyploidy. Nevertheless, the four instances dis- cussed suttee to indicate that the role of polyploidy in the evolution of bisexual animals should no longer be completely denied.

~UMMAI~u 1. The possible conne~on between muRiple sex-chromosome mechanisms and poly- in Forficuiina, Gryllotalpa, spp., Pentatonfidae and Mantidae is discussed. 2. Fo'r/icula smyrnensis Serv. (2,n=21) has an X1X,zY mechanism and thus belongs to the group of Forficulina which combine tetraploidy with a multiple sex mechanism. 3. it is shown that an X1X2Y mechanisn~ might arise as the direct result of a single paracentric inversion in the tetraptoid (XX, YY) male germ-line.

I~EFEI~ENCES B~uneozzi, C. (1946). 0ber die geographische VerbreRung der Mutanten yon Artemia scdina Leach. Arch. Klaus-Stifl. Vererb&orsch. 21. BAvn~,I-L(1947). KuryologischeNotizcn. L Ubergener~tivePolyploidiebeiDermapteren. Z, lYat'lt,rf. 2b. C~L~, ]t. G. (1941). The sex-determining mechanism of the earwig l~'o~:ficuh~a, uricularia. J. Genet. 41. GOLDSOILMIDT,E. (1946). 1)olyp]oidy ~nd parthenogenesis in the genus s iVature, Lend., i58. Guess, I0. (1932). Untersuehungen iiber die Polyploidie und die Variabilitttt bei Artemia saline. Ncdur- wissenschaflen, 20. 440 M%lt@le sex-chromosome mechanisms and polyploidy in animals ]=[UClIES-SOItl~AD]~1%S. (19,I3a). without, chiasmata in diploid and tet,raploid spermaLocyges of l,he mantid Callimantis antillarum Saussure. J. Morph. 73. H[rc'g~s-Sonr~ADm~, S. (1943b). Polarization, kinetochore movements End structure in the meiosis of male mangids. Biol. Bull., Wood's Hole, 85. l(usn~n~, T. (1948). Ctn'omosomal evolution in the European mole-cricket. , Lend., 161. Kl~sttm~, T. (1952). I-]:eterocln'omatic in Gryllolalpa gryllohdpa, L. J. aenet. 50. hla'r'm~s~, R,. (1946). D&nonsbr'~tion du caractgre ggographique de la parthdnogen~se do Pallas eL de sa polyploidic. Experientia, 2/7. ]ga'ra'i~m~, (1946). Communications prgliminMres sur les chromosomes des P16eopt6res. Experientia, 2/12. McCLI:N~'oot~, ]3. (] 941 ). Spontaneous alterations in chromosome size and tbrnl in Zec~ mays. Cold Npr. Harb. ~gymp. @la,nt. Biol. 9. McOr, u~c,, 0. E. (1939). Chromosome numbers in animals, ff'abul, biol., Berl., t8, pars 1. i~CECE:~~, G. [:[. (19-'t5). S~apsis End behavior of' chronmsomes in polyploid male germ cells of Romalea mieroptem ]3eauv. , 30. Mvsn~, ]-L J. (1925). Why polyploidy is rarer in animals than in plants. Amer. Nat. 59. Snlr~]m, J. (1948). The origin of parthenogenesis in the Psyclfids. Eighlh ~rnt. Genet. Contr. Abstract Boo]< Suo~nt~trs~sr, E. (1940). Polyploidy in parthenogenetic Cureulionidae. Hereditas, Lurid, 24. Suo~rAr~rt~nsr, E. (1948). Parthenogenesis and polyploidy in weevils, Cnreulionidae. Eighth Int. Genet. Congr. Abstract Boo/< V~tNDn5, A. (1946). Le r61e de la polyploidie dens le rSgne animal. Arch. Klaus-Stift. VererbForseh. 21. V~t~Dnn, A. (1947). Sur la g6n6tique et la sexualit6 des Isopodes terrestres. X. ]~tude des gamfitures etu'omosomiques de quelques espSces d'Isopodes marins, duleaquieoles eg terrcstres. Bull. biol. 8t. Wma'n, M. J. D. (1938). A new End anomalous type of meiosis in a mantid, Callimantis antillarum Saussure. Prec. JRoy. Nee. ]3, t25. WroTh, M. J. D. (1940@ The origin and evolution of multiple sex-clu'omosome mechanisms. J. aenet. 40. Wm'r~, M. J. D. (1940b). Evidence for polyploidy ill the hermaphrodite groups of animals. Nat~tre, Lend., 146. Wtr~, h'[. J. D. (1941). The evolution of the sex-elu'omosomes. I. The XO and XtX~Y mecha~fisms in prayh~g mantids. J. Genet. 42. Wm'r~, B'[. J. D. (1945). Animal Cytology and Evolution. Cambridge.

Since this paper was sent to the press, the following papers with a possible bearing on the discussion have come to the author's notice: Ocs I-I. A. (1950). Clu.omosonles et l:t6tdrochromosomes de Tdn6brionid6s. Genetica, 25. ]-IUs S. (1950). Tim ehromosonms of mantids (Orthoptera: Mantidae) hi relation to taxonomy. Chromosoma, 4. ttuo~Es-Son~,~o~, S. (1951). The desoxyribonucleic content of the nucleus as a oyLotaxonomic ehal'acter in mantids (0rthoptera: Mantoidca). Biol. Bull., Wood's Hole, 100. ~{ANNA, ~. K. (1951). A study of the ehronmsomes during meiosis in forty-tlu'ee species of Indian tleteroptel'a. Prec. Zool. ~oc. Bent. ~. M~Ta'llm~, 1~. & A~zsm~T, J. (1947). Los chromosomes des P16coptgres. Bull. biol. 8t.

For full lists of the known chromosome nmnbers in Pentatomidae (Table 3) and in Mantidae (Table 4), respectively, the following refm'enccs shonld be consulted: h'L~I~INO, S. (1951). Chromosome Numbers in Animals. Iowa College SLate Press. MAN~A, G. K. (1951). Cf. above. tIvG'in~s-Som~:~DEn, S. (1950). Cf. above.