Heredity 55 (1985) 167—174 The Genetical Society of Great Britain Received 10 January 1985

The genetics of and homostyly in Turnera ulmifolia L. (Turneraceae)

Joel S. Shore and Department of Botany, University of Toronto, Toronto, Spencer C. H. Barrett Ontario, Canada M5S 1A1.

Turnera ulmifolia L. is a polymorphic complex of diploid, tetraploid and hexaploid varieties. Diploids and tetraploids are distylous and hexaploids homostylous. A controlled crossing programme demonstrated that in diploids distyly is controlled by a single locus with two alleles. Long-styled plants are ss and short-styled plants can be either Ss or SS. In tetraploids a similar pattern occurs with short-styled p!.ants usually Ssss and long-styled plants ssss. Tetrasomic inheritance was demonstrated by crosses with a SSss genotype synthesised by coichicine doubling. Double reduction could not be detected at the distyly locus. No significant deviation from a 1: 1 morph ratio was observed in surveys of nine natural populations and progeny tests of 21 open-pollinated familes from Brazil. Crosses between distylous and homostylous populations were undertaken to determine the inheritance of homostyly. The results were consistent with a model of control. Clear segregation of was observed in the F1, and the dominance relationships S> h> s, where h is an allele that determines homostyly, were obtained.

INTRODUCTION Turnera ulmfolia L. is a polymorphic assem- blage of perennial weeds native throughout the Distylyoccurs in at least 23 flowering plant families Neotropics. Urban (1883) deseribed 12 varieties (Ganders, 1979) and has undoubtedly evolved within the complex, six of which are distylous and several times. The inheritance of distyly has been the remainder homostylous. Barrett (1978) determined for species in 11 genera from nine described the floral biology and breeding systems families (Ornduff, 1979). The syndrome of floral of four varieties within the complex, and a recent characters, by which the long- and short-styled survey of numbers in 43 populations morphs differ, is inherited as if controlled by a of T u1mfo1ia (Shore and Barrett, 1985; and single locus with two alleles. Except for two unpublished data) revealed a correlation between genera where the dominance relationships are breeding system and ploidal level. All distylous reversed (Baker, 1966; Ornduff, 1979), the long- populations are diploid or tetraploid, whereas styled morph is homozygous (ss)whilethe short- homostylous populations are hexaploid. Here we styled morph is heterozygous (Ss). Evidence from investigate the genetics of breeding system vari- the (Ernst 1955), and the Plum- ation in the T ulm(folia complex. Specifically we: baginaceae (Baker, 1966) suggests that distyly is (1) determine the inheritance of distyly in diploids controlled by a series of tightly linked com- and tetraploids; (2) provide data on morph ratios prising a supergene. Aberrant forms termed and segregation from natural populations; (3) homostyles, with anthers and stigmas at the same determine the inheritance ofhomostylyand discuss level within a flower, are interpreted as recom- evidence for supergene control of distyly. binant phenotypes that arise by crossing over within the supergene. A recombination event resulting in homostyly has, however, never been MATERIALSAND METHODS detected in heterostylous species (Charlesworth and Charlesworth, 1979a). In addition, apart from a Acrossing programme was undertaken on glass- few notable exceptions (Crosby, 1949; Ernst, 1955; house grown plants raised from seed collections Ganders, 1975), homostyles are rarely observed in or cuttings obtained from natural populations. distylous populations, although relatives of Table 1 gives the locality, chromosome number heterostylous taxa are frequently homostylous. and varietal status of accessions used in the study. 168 J. S. SHORE AND S. C. BARRETT

Table IVarietal status, ploidal level, and locality of Turneraulmtfolia accessionsused in experimental studies (X =5)

Ploidal Population Variety level Locality Collection No.

11 intermedia 2X Barreirinhas, Brazil Barrett 1128 13 intermedia 2X Caracas, Venezuela Barrett 1125 16 intermedia 2X Managua. Nicaragua Barrett 1342 124 intermedia 4X St. (ristohal, Dominican Rep. Barrett and Shore 1364 132 intermedia 2X Arco Verde, Brazil Barrett and Shore 1374 ES elegans 4X Crato, Brazil Barrett 222 Eli elegans 4X Salgueiro, Brazil Barrett and Shore 1372 AS angustifolia 6X Ochos Rios, Jamaica Barrett 1253 All angusti fo I ia 6X Dragons Ray, Jamaica Barrett 1259 A17 a ngusti Co Ii a 6X Pelican Lake, Grand Bahama Correll 40638 01 orientalis 6X Corrientes, Argentina Arho 1538 Vi velutina 6X Tuxtla Gutierrez, Mexico Koch & 1-ryxell 7834i

Each individual was given a code indicating its and a short-styled plant were selected for accession, or family if applicable, followed by a reciprocal crosses. To determine the inheritance of numeric value specifying the particular individual homostyly, three homostylous varieties, from five within the accession, and by a letter indicating its accessions of T. ulmijhlia, were crosed to diploid (L =long-styled,S =short-styled,H = long- and short-styled plants of known genotype. homostyled).All pollinations were performed in To examine the equilibrium frequency in T. a pollinator-free glasshouse using fine forceps. u1mifilia we extend the morph frequency data of Flowers were emasculated prior to cross-pollina- Barrett (1978) by sampling a total of 1211 plants tion. Pollinated flowers were individually marked from nine natural populations of the tetraploid T. and maturing capsules were wrapped with parafllm ulmifolia var. elegans in N.E. Brazil. Random or to prevent loss of seeds during dehiscence. As complete samples of populations were taken with distylous members of the complex are strongly at least 90 plants sampled per population. Further, self-incompatible two different methods were used progeny tests of 21 open-pollinated families, col- to obtain seeds from self- or intra-morph crosses: lected from population El I in Brazil were per- (1) flower buds were opened one day prior to formed to test for heterogeneity among families anthesis and pollinated from an open flower of the and among maternal morphs. On average 62 pro- same individual (hud-selfing), (2) plants were geny were scored for each family. screened for the presence of a weakened incom- All goodness-of-fit and heterogeneity tests were patibility reaction (pseudo-compatibility) and performed using the G statistic (Sokal and Rohif, those yielding more than three seeds per pollina- 1981). tion were later used in the crossing programme. Progenies obtained from crosses were grown to flowering in individual pots. RESULTS To investigate the inheritance of distyly at diploid and tetraploid levels accessions comprising Neitherof the two methods employed to obtain different varieties were employed (table 1). seed from selfing long- or short-styled plants was Reciprocal crosses were generally performed and completely successful. Bud-selfing in T. ulm(fo!ia the results pooled. Preliminary results suggested results in seed set more often in short- than long- that short-styled morphs were of genotype Ss. To styled individuals; only one of many long-styled detect the occurrence of SS genotypes, 19 short- plants yielded seed. In both morphs the yield of styled progeny derived from the self of 132-1 S were seed from bud-selfing is less than 75 per cent of selfed and at least 17 progeny from each family that from legitimate pollinations. Screening plants were grown to flowering and scored for floral for pseudo-compatibility resulted in the recovery morph. To investigate the possibility of tetrasomic of a few individuals that produced sufficient seed inheritance and double reduction, the chromosome on self-pollination to he useful for genetic study. number of seedlings derived from the cross 132-IS x Two plants were identified among diploids (1311- Il-IOL, was doubled. A drop of 0l per cent col- 3L and 132-iS) and two among tetraploids (ES-IL chicine applied to cotyledons resulted in the and ES-los). Progeny (>80 per cross) derived by recovery of several tetraploid plants and a long- selfing or crossing plants ES-IL and ES-lOS were GENETICS OF HOMOSTYLY 169 screened for self-compatibility. Six progeny Four of 19 short-styled plants, derived by yielded sufficient seed for further study. selfing plant 132-iS, yielded no long-styled pro- geny upon selfing. At least 34 selfed progeny were Inheritance of distyly in diploids scored for each of these four plants. The probabil- (i) ity of observing no long-styled plants among the Theinheritance of distyly in diploid T. ulmifolia progeny of a heterozygous parent for a sample size var. intermedia was determined using three long- of 34 is less than 6 x i05. Hence these individuals and six short-styled plants, from four different are likely to be short-styled plants of genotype SS. accessions, and one long-styled plant (1311-3L), Among the segregating progenies, 105 long-styled from the cross 13-3Sxll-1OL. Bud pollinations and 326 short-styled plants were obtained and no were used for all illegitimate crosses except those deviation from 1: 3 or heterogeneity, was observed involving individuals 1311-3L and 132-iS which (Gdev= 009,P =076; Ghet = 178,P =0.22).The yielded sufficient seed on selfing. The data presen- occurrence of four non-segregating plants as well ted in table 2 are consistent with the common as the absence of a deficiency in short-styled pro- geny from selfs of short-styled plants indicates that Table2Style morphs in progeny of crosses of Turnera SS genotypes are viable. ulrnifolia var.iniermedia (2n = 10)

Style morphs of (ii,)Inheritance of distyly in tetraploids progeny Atthe tetraploid level plants from two accessions Cross Long Short G P were used, one each from vars. elegans and inter- media. Bud-selfing was employed for individual (a) Legitimate crosses 124-iS only. All other plants were selfed. I6-l2Lxl6-19S 34 58 633 001 16-l2Lxl6-31S 65 53 122 027 Individuals SS3S and SS77S are self-fertile sibs 16-l2Lxl3-3S 90 78 086 036 obtained by selfing E5-IOS and screening several 13-3S x13-4L 16 23 126 026 of its progeny for pseudo-compatibility. Plants 13-24S x 13-4L 9 9 000 — SL34S and SL36L were similarly obtained from ll-2S xIl-IOL 26 18 146 023 the cross E5-1OSxE5-IL and plants LL61L and Deviation from 1: 1 G =0002,P =096 Heterogeneity G =11138,P =005 LL51L from the self of ES-iL. Data in table 3 indicate that short-styled plants are heterozygous (b) Illegitimate crosses of the short-styled morph 16-19S x l6-31S 4 29 340 007 and long-styled plants are homozygous. Aberrant 16-19S selfed 3 15 073 039 ratios were obtained in four crosses. The parental l6-31S selfed 5 18 013 071 short-styled plant ES-lOS yielded an extreme 13-24S selfed 5 13 007 079 deficiency of short-styled progeny on selfing, as 13-3S selfed 21 52 054 046 did two of its three progeny (SS77S and SL34S). 132-iS selfed 33 109 024 063 Deviation from 1:3 G =058,P =045 To account for the aberrant ratios from these Heterogeneity G=452, P=050 three selfs, three models with different expectations (c) Illegitimate crosses of the long-styled morph were investigated. Since the crosses gave l6-12L selfed 52 0 — — homogeneous segregations (G =058,P> 0.5) 13l1-3L selfed 156 0 — — results were pooled, giving a ratio of 1 long: 123 short. The models evaluated were: (1) a model assuming a maximum amount of double reduction, genetic model of the inheritance of distyly. Short- corresponding to random chromatid segregation styled plants are heterozygous (Ss), yielding both (Allard, 1960), with an expectation of 1 long:2.48 morphs on selfing, and long-styled plants are short (G =527,P <0.001); (2) a model assuming homozygous (ss) with only long-styled plants in lethality of zygotes containing more than one S selfed progeny. Heterogeneity was apparent allele giving an expectation of 1 long: 2 short (G = among legitimate crosses. This was largely the 258,P<0001); (3) a model assuming both a result of the cross (16-12LxI6-19S); the only maximum amount of double reduction and example showing heterogeneity among lethality of zygotes carrying more than one S allele, reciprocals. When the short-styled morph was used with an expectation of 1 long: 16 short (G =772, as the parent a large excess of short-styled P<0.01). None of the models accounts for the progeny was observed. Further we note that all extreme deficiency of short-styled plants, but the crosses involving plant 16-19S yielded an excess third comes closest to the observed ratio. Evidence of short-styled plants. reviewed below, however, indicates that double 170 J. S. SHORE AND S. C. BARRETT

Table 3Style morphs in progeny of crosses of Turnera Table 4 Stylemorphs in progeny of open-pollinated families ulm(folia vars. elegans and interinedia (2n —20) of Turnera u1mftilia var. elegans (2n =20)from Brazilian population (Eli) Style morphs of progeny Style morphs of progeny

Cross Long Short G P 1-amily Long Short

(a) Legitimate crosses 51 39 43 ES-I Lx ES-lOS 91 76 135 025 S2 12 7 124-3L x F.5-1OS 71 96 376 005 S3 25 27 Deviation from1:1 6—030, P=058 S4 10 15 Heterogeneity 6=481, P—0•03 S5 39 34 56 29 22 (h) Illegitimate crosses of the short-styled morph S7 6 8 S 31 051 124-IS selfed 044 S8 10 9 ES-lOS selfed 79 100 3089 <0001 S9 23 27 SS3S selfed 29 66 148 022 SIt) 29 23 5S77S selfed 56 61 2838 <0•001 SIl 49 52 SL34S selfed 67 87 2494 <0•001 Deviation from 1 3 G — P <0001 LI 7090, L2 63 69 Heterogeneity G— 1523, P0004 L3 46 49 (c) Illegitimate crosses of the long-styled morph L4 35 42 ES-iL selfed 130 0 — L5 35 30 SL36Lselfed 147 0 — L6 9 16 LL6ILselfed 14 1) L7 8 14 LLS1L selfed 6 0 L8 57 63 L9 39 35 (d) Legitimate cross of synthetic tetraploids Ll0 71 72 SNISXLNIL 35 208 — Deviationfrom 1:5 6— 093, P —033 df 6 P Deviation from 1: 1 1 031 058 reduction may not occur at the distyly locus and Between morph heterogeneity 1 048 049 19 968 094 hence the model may be inappropriate. Between family heterogeneity The synthetic tetraploids produced by somatic chromosome doubling had genotypes SSss (short- were highly sterile. Sterility precluded the possibil- styled) and ssss(long-styled).On crossing, the progeny showed no deviation from the expected ity of examing further generations. However, clear 5 short: 1 long tetrasomic ratio (table 3(d)). A floral dimorphism was evident among progenies maximum likelihood estimate and standard error (fig. 1(a), (h)), despite morphological divergence of the double reduction parameter a was obtained and sterility barriers among the diploid and hexa- jointly from these data and the pooled data from ploid varieties. In each of the three homostylous open-pollinated families of var. elegans (table 4). varieties that were examined, no long-styled plants The estimation procedure yielded a value not sig- were obtained in crosses. However, crosses that nificantly diflerent from zero (a =—0045,s.c. involved short-styled plants always segregated 0044). Hence double reduction could not he detec- both short-styled plants and homostylous plants ted at the distyly locus. at equal frequencies (table 5). On the basis of these patterns of segregation an apparent homostyle Style morph frequencies in natural populations allele (h), which is dominant to the long-styled ofvar. elegans in Brazil were homogeneous (Giet= allele (s), but recessive to the short-styled allele 7.23,P =0.51)and reveal no significant deviation from I : I expectation (G,jev= 007,P —0.79). The (S), governs the homostylous phenotype in T. ulmifolia. 21 open-pollinated families sampled from a natural All homostyles of T. ulmijolia that we have population in Brazil (Eli) of var. elegan.s (2n =20) provided no evidence of deviation from 1: examined exhibit the floral phenotype of a long- homostyle, with long styles and long-level anthers. expectation or heterogeneity among morphs or However, considerable variation occurs in the rela- families within morphs (table 4). tive lengths of reproductive organs among popula- tions, with some displaying a considerable degree (iii) The inheritance ofhomostyly of herkogamy. Further details on the nature of the All F1 progeny obtained from crosses between variation and its genetic basis will be presented homostylous hexaploids and distylous diploids elsewhere. GENETICS OF HOMOSTYLY 171

17 21 A. B.

- E14— S 18 A H E .. H 2. Agg S. AA J. LitAA A LA A II- '5 AM A f A C Q) E 08 12-

C,)

5 9 5 8 II 14 17 9 12 5 18 21 Style length (mm.) Figure 1Distribution of floral phenotypes in crosses betweendistylous and homostylous populations of Turnera ulmfolia (a) Ol-21H x16-19S (b) Al1-12H x132-lS.

DISCUSSION

Table 5 Style morphs in progeny of crosses of distylous Tur- Thegenetic control of distyly was first elucidated neroulmfolia var. intermedia (2n =10)with three homsty- by Bateson and Gregory (1905), although Darwin bus varieties (2n =30) (1877) undertook the necessary crosses. In all cases, the syndrome of characters that comprises Style morphs ofprogeny the is controlled by a single gene Cross Long Short Homostyle locus with two alleles. Recently, Schou and Philip (1984) have identified a second genetic system (a) crosses with var. angust(folia where the floral polymorphism and incompatibility (i) Homostyle x Short A1l-12HxI32-1S 0 54 46 system are apparently uncoupled, and possibly A11-12HxI6-19S 0 17 14 controlled by unlinked loci. A similar system may A11-12Hx16-31S 0 11 18 operate in Narcissus (Dulberger, 1964). Evidence A1l-14Hxl32-1S 0 10 3 for supergene control of distyly has been obtained A1l-14H >U6-l9S 0 7 9 for species in the Primulaceae (Ernst, 1955) and A5-28H x132-lS 0 3 5 Deviation from iS: 1H G=025, P=062 Plumbaginaceae (Baker, 1966). Preliminary data Heterogeneity G712, P021 is also available for the Rubiaceae (Baker, 1958). In Amsinckia spectablis of the Boraginaceae, (ii) Long x Homostyle 16-l2LxAll-12H 0 0 4 Ganders (1979) has shown that homostylous 16-12LxA11-14H 0 0 4 phenotypes are not the result of recombination 16-12LxAI7-1H 0 0 7 within a supergene. This does not exclude the (b) crosses with var. orienialis possibility of supergene control of the polymorph- 16-12Lx01-21H 0 0 80 ism in this species, but indicates that genes other O1-21H xlo-19S 0 40 36 than those of the supergene are responsible for Deviation from IS:1 H G =021,P =065 homostyle formation. Indeed, two such genes are known to occur in sinensis (Mather, 1950). (c) crosses with var. velutina The Turnera ulmfo/ia complex exhibits distyly, V1-3HxI32-1S 0 2 2 Vl-3H x16-19S 0 0 1 with reciprocal lengths of styles and stamens, pol- l1-IOLxV1-3H 0 0 4 len size dimorphism, and a strong self- and intra- morph incompatibility system (Barrett, 1978). In 172 J. S. SHORE AND S. C. BARRETT diploids, we have shown that distyly is controlled were used to determine the inheritance of by a single locus with two alleles. Long-styled homostyly and provide evidence for supergene plants are ss and short-styled plants can be either control of distyly. Based on a hypothesis of super- Ss or SS. However, homozygous shorts, although gene control of distyly we can predict (1) discrete viable, will not generally occur in natural popula- phenotypic segregation and (2) specific dominance tions, as disassortative mating, enforced by dial- relationships of alleles governing control of the lelic incompatibility, will prevent their formation. alternative floral phenotypes. Under the model we In tetraploids of T ulmfiliaasimilar pattern of expect the following dominance relationships: S> inheritance is observed. Short-styled plants are of h> s, where h is an allele determining homostyly. genotype Ssss and long-styled plants are ssss. A This pattern of dominance was observed for short-styled plant of genotype SSss was syn- crosses involving all three varieties, although for thesised by colchicine doubling and presumably var. velutina few progeny were raised. The clear short-styled genotypes with 3-4 doses of the S segregation of floral phenotypes in the F1 and allele could be synthesised by the appropriate pro- pattern of dominance is consistent with the cedures. hypothesis that distyly is controlled by a supergene A large deficiency in the number of short-styled (composed of at least two loci) in T u1mif1ia. progeny was obtained on selfing short-styled plants The similar behaviour of homostylous varieties, of the tetraploid T. ulrn(ThIia var. elegans. This in crosses with heterostylous populations, suggests occurred in a self-compatible short-styled plant that they have arisen via the same genetic mechan- and two of its progeny. None of the three models ism involving recombination within the distyly considered gave a satisfactory fit to the data. We supergene. Charlesworth and Charlesworth suggest that the aberrant ratios may he the result (1979a) modelled the breakdown of distyly and of the self-compatibility gene(s) imparting a selec- found that if the allele determining the short-styled tive advantage to male gametophytes of genotype niorph is dominant, as in C ulmiJilia, long-homo- s.c. This hypothesis could be tested by performing styles are likely to spread to fixation with greater the appropriate crosses. Aberrant ratios and their probability than other self-compatible phenotypes. possible causes have been considered for other Data from T u/rnifolia provide support for the heterostylous taxa (Mather and de Winton, 1941; model since each breakdown event has resulted in Baker, 1975; Weller and Ornduff, 1977; Ganders, fixation of the long-homostyle phenotype. 1979). In our surveys and experimental work of disty- Casper and Charnov (1982) argue, based on bus populations in T. u/m,Thlia we have not sex allocation theory, that the 1: 1 morph ratio observed the occurrence of homostylous plants. found in most distylous populations is an Mather (1950)proposedthat the supergene con- evolutionary stable state. Further, under their trolling distyly in Prirnula might he contained model "autosomal" genes can cause the ratio to within an inversion and as a result was protected deviate from 1: 1 given the appropriate selection from recombination. However, no firm evidence pressures. In nine populations of C u/rn ifolia var. that such an inversion occurs in Prirnula species elegans we found no evidence of deviation from has been found and we have no cytological a 1: 1 morph ratio. In addition, progeny tests of evidence for inversion polymorphisms in T. 21 open-pollinated families revealed no deviation ulmifolia. De Winton and Haldane (1935) found from 1: 1, or heterogeneity among families. These no evidence for double reduction in P. sinensis data suggest that no significant genetic variation and Dowrick (1956) detected a low frequency of for morph ratio occurs within these populations occurrence in P. obcon lea. Since this may indicate of T. ulrn(foliavar.elegans,andisoplethy is a that the distyly locus is linked to the centromere, simple outcome of disassortative mating and Dowrick (1956) suggested that centromere inter- Mendelian segregation at the distyly locus. ference might prevent crossing-over from occur- The three homostylous varieties of T. u1rnfi!ia ring within the supergene of some Prirnula species. that we have studied experimentally are mor- We have demonstrated tetrasomic inheritance phologically differentiated, allopatric, intersterile, of distyly in tetraploid C ulmifolia, however, we and occur at different margins of the range of the did not detect double reduction. The frequency of species complex. This suggests that heterostyly has double reduction is an increasing function of the broken down to homostyly on at least three frequency of quadrivalent formation and recombi- occasions in the species complex, always in associ- nation between the locus and centromere. Quad- ation with the hexaploid condition (Shore and rivalent formation has been documented in tetra- Barrett, 1985; and unpubi. data). All three varieties ploid C ulmifolia (Raman and Kesavan, 1964; GENETICS OF HOMOSTYLY 173

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