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Evidence for Female Heterogamety in Two Terrestrial Crustaceans and the Problem of Sex Chromosome Evolution in Isopods

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Evidence for Female Heterogamety in Two Terrestrial Crustaceans and the Problem of Sex Chromosome Evolution in Isopods Heredity 75 (1995) 466—471 Received 14 February 1995 Evidence for female heterogamety in two terrestrial crustaceans and the problem of sex chromosome evolution in isopods PIERRE JUCHAULT* & THIERRY RIGAUD Université de Pa/tiers, Laboratoire de Biologie An/male, URA CNRS 1975, 40 avenue du Recteur Pineau, F-86022 Poitiers Cedex, France Femaleheterogamety (WZ type) has been demonstrated in the terrestrial isopods Oniscus asellus (Oniscidae) and Eluma purpurascens (Armadillidiidae), by making crosses between two genetic females (one of them experimentally reversed into a functional neo-male). The WW individuals generated by such crosses were viable and fertile females. These data, plus the frequent monomorphism of sex chromosomes and the coexistance of two heterogamety types (XX/XY and WZ/ZZ), indicate that sex chromosome differentiation in isopods is at a prim- itive stage. The evolution of sex chromosomes in this group of crustaceans is discussed, and it is suggested that this evolution has been disturbed by parasitic sex factors. Keywords:Elumapurpurascens, heterogamety evolution, Oniscidea, Oniscus asellus, sex deter- mination, sex-ratio distorters. Introduction tacea and are only known in three species: the bran- chiopod Artemia sauna (Bowen, 1963) and two Ourpoor knowledge of sex determining mechanisms marine isopods, Idotea baithica and Dynamene biden- in crustacea results from, in considerable measure, tata (Table 3). Female heterogamety (WZ) has been to the difficulties in establishing the heterochromo- demonstrated in these three species by crossing indi- somic sex in this group. Such knowledge is essential viduals exhibiting genetic polychromatism. for assessing the evolution of sex determination, par- Reversing genetic females into males (creating ticularly in terrestrial isopods where sex determina- neo-males) by the early implantation of the andro- tion is often disturbed by parasitic elements genic gland is an accurate method by which hetero- (Juchault et al., 1993, 1994). Heterogametic mechan- gametic sex can be determined. Such crosses have isms have been demonstrated in gonochoric crusta- demonstrated female homogamety (XX) in the ceans by three methods: cytogenetics, sex-linkage of amphipods Orchettia cavimana and 0. gammarellus markers and crosses between females and neo-males (Ginsburger-Vogel, 1972, 1973) and in three terres- (experimentally reversed females) (review in Gins- trial isopods: Porcellio dilatatus dilatatus, Armadilli- burger-Vogel & Charniaux-Cotton, 1982). dium nasatum and Helleria brevicornjs (Table 3). Karyotypic analysis is often difficult because of the Female heterogamety has been shown in the Onisci- large number of small chromosomes in many crusta- dea Annadiiidiu,n vulgare, Porcellio dilatatus petiti, cean species. This is the case in terrestrial isopods and in the Valvif era Idotea baithica. Cytogenetic (Oniscidea) in which the diploid number varies from studies failed to show any morphological differentia- 16 to 94 often being as great as 50, and chromo- tion of heterochromosomes in some of these species somes rarely exceed 2 pm in length (Artault, 1977). (Artault, 1977; Table 3). Only one case of a cross Nevertheless, sex chromosomes have been identified between a female and a neo-male has been reported morphologically in a few species of isopods (see for Crustacea other than the Peracarida. This was in Table 3). the prawn Macrobrachium rosenbergii, in which the Although few species have been extensively females are heterogametic (WZ) (Malecha et a!., studied, sex-linked genes appear to be rare in Crus- 1992).Successful matings of two andrectomized males (=neo-females)with normal males of this *Correspondence species have provided further evidence of male 466 1995 The Genetical Society of Great Britain. HETEROGAMETY N ISOPOD CRUSTACEANS 467 homogamety (ZZ) (Sagi & Cohen, 1990). Never- The sex ratio did not deviate from 1:1 in control theless, the finding of unexpected sex ratios among crosses (x2testnonsignificant in all cases). The sex crosses implies that 'the genetic determination of sex ratio was always female-biased in crosses involving in prawns must be more complicated than a simple neo-males ('experimental' crosses), and never signifi- female-heterogametic mechanism' (Malecha et al., cantly different from 1/3 (f-test). The 17 F2 from 1992). three different 'experimental' F1 produced either This paper describes the results for two terrestrial broods with a balanced sex ratio (10 crosses, produc- isopods showing female heterogamety. The results ing 130g/119?), or all-female broods (seven crosses, have been integrated into previously obtained results producing 0/147) (Table 1). to provide a clearer picture of sex chromosome evo- lution in this group of crustaceans. Elumapurpurascens Eightmales and four neo-males from the same F0 Materialand methods progeny were crossed with their sister. The results TwoOniscidea species were investigated: Oniscus were similar to those for 0. asellus. The sex ratios of asellus (Oniscidae) and Eluma purpurascens (Arma- the broods were balanced in control crosses, and dillidiidae). Oniscus asellus were collected in a gar- female-biased (1I3) in 'experimental' crosses. The den at Celles-sur-Belle (Deux-Sèvres, France) and eleven F2 from one 'experimental' F1 produced E. purpurascens in woodlands near Sepvret (Deux- either amphogenous broods(eightfamilies; Sèvres, France). Progeny obtained from wild gravid females (F0 progeny) showed a 1:1 sex ratio (results not shown, but see control crosses in Tables 1 and Tabte 1 Sex ratio in offspring of Oniscus asellus 2). Feminizing Wolbachia infection similar to that observed in many isopod species (Martin et a!., 1973; F1 F2 Juchault et al., 1994) was not detected, by either Family no. electron microscopy or PCR (Juchault et a!., 1994). Family no. These preliminary results indicate that sex in these 1 11 13 Aa 8 6 populations of Q asellus and E. puipurascens is 2 5 9 Ab 16 6 probably not under the control of non-Mendelian 3 24 17 Ac 23 16 genetic elements (Legrand et aL, 1987). 4 11 12 Ad 14 9 The heterogametic sex was diagnosed by breeding 5 10 8 Ae 9 10 animals whose sex has been experimentally reversed 6 11 17 Af 0 27 by hormone treatment, using the technique of 7 10 10 Ag 25 26 Juchault & Legrand (1964). Full-sib very young Ah 10 5 females (4 mm in 0. asellus; 3 mm in E. purpur- Ai 0 24 Aj 0 21 ascens) were implanted with one androgenic gland A 5 18 from an adult male. The androgenic glands (organ B 3 15 Ba 0 13 responsible for male hormone synthesis) survived in C 6 20 Bb 15 20 their new hosts, and continued to produce male hor- D 5 22 Bc 5 11 mone (Juchault & Legrand, 1964). The implanted E 2 13 Bd 0 18 females became neo-males 350 days after the F 5 19 implantation. These neo-males are thus chromo- G 7 21 somic females with a male phenotype, male behav- Ca 0 11 iour and male physiology. They were crossed with Cb 0 33 their intact (normal) sisters, and produced F1 Cc 5 10 females progeny. From these F1, full-sib males and In the first generation (F1), the family numbers 1—7 were crossed to obtain the F2 generation. denote crosses between a normal male and one of its sisters (control crosses), while families A—G denote crosses between a neo-male (see text) and one of its Results sisters ('experimental' crosses). In the second generation Oniscus asellus (F2), families begining with the same capital letter indicate crosses between full-sib individuals from the same Seven normal males and seven neo-males from the F1 progeny. Vertical bars indicate crosses in which one same F0 progeny were crossed with a full-sib female. male was mated with two or three females. The Genetical Society of Great Britain, Heredity, 75, 466—471. 468 P. JUCHAULT & T. RIGAUD Table 2 Sex ratio in offspring of Eluma purpurascens gamety in a species is rare, but has been reported for Chironornus tentans (Diptera) (Thompson & F1 F2 Bowen, 1972) and the platyfish Xiphophorus (Gor- don, 1954; Kaliman, 1965). Our data indicate that Family no. Family no. the heterogametic system is not yet fully established in the Isopoda. 1 9 12 Aa 0 41 Oniscus asellus and E. purpurascens WW females 2 11 21 Ab 31 30 3 16 25 Ac 21 29 are viable and fertile. The viability of such an 4 22 37 Ad 16 18 unusual genetic combination has also been reported 5 17 23 Ae 17 21 for the Oniscidea Armadillidium vulgare and Porcellio 6 24 21 Af 0 38 dilatatus, and for the amphipod Orchestia gammar- 7 35 33 Ag 16 15 ellus (Ginsburger- Vogel & Magniette-Mergault, 8 30 23 Ah 24 19 1981). The sex chromosomes in these species must A 7 25 Ai 0 8 have large homologous segment, for there to be B 2 10 Aj 5 5 such viability. This contrasts with the situation in C 7 18 Ak 13 21 mammals and insects, where the sex chromosomes D 11 37 are often so differentiated that YY individuals are This table follows similar conventions to those in Table 1. inviable or sterile (Bull, 1983). It is generally accep- ted that the morphological similarity of the sex chromosomes indicates a relatively early stage of 143/158) or all-female broods (three families; specialization of a pair of ancestral chromosomes 0/87) (Table 2). carrying sex determinants (Bull, 1983; Charlesworth, 1991). The isopod group may well fall in this cate- gory. There are only tiny morphological differences Interpretation between the sex chromosomes in Porcellio rathkei Asthe results for both species were similar, crosses and P laevis (Mittal & Pahwa, 1980, 1981), and in these two isopods can be interpreted in the same incipient sex chromosome differentiation has been way. Crosses involving neo-males can be seen as proposed to account for the slight morphological crosses between two heterogametic (WZ) difference in the male-specific chromosome in Asel- individuals: lus aquaticus (Rocchi et a!., 1984).
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