Breeding System Evolution in Primula Vulgaris and the Role of Reproductive Assurance

Heredity 56 (1986) 207—217 The Genetical Society of Great Britain Received 15 July 1985

Breeding system evolution in Primula vulgaris and the role of reproductive assurance

J. G. Piper, B. Charleswortht School of Biological Sciences, University of Sussex, and D. Charleswortht Falmer, Brighton BN1 9QG.

Reproductive assurance in the absence of pollinators has frequently been discussed as a major factor in the evolution of seif-fertilisation. An attempt was made here to assess the importance of this factor in the evolution of the self-fertile homostyle morph in Somerset populations of P. vulgaris by a comparison of the relative fertilities of homostyle and outcrossing (pin and thrum) morphs. Several indices of fertility indicated that at some populations in some seasons homostyles were significantly more seed fertile than the pins and thrums. This trend in relative fertility made it clear that reproductive assurance could have had a profound effect on the evolution of seif-fertilisation in this species. The proximate cause of variation in relative fertility was shown to be variation in pollinator service due to differences in rainfall between seasons. Factors such as sexual resource reallocation, reproductive economy, and inbreeding depression were not shown to have a significant effect on the relative fertility of the seif-fertilising and outcrossing morphs.

INTRODUCTION vulgaris over a wide range of frequencies, (Crosby, 1949; Curtis and Curtis, 1985). It has achieved a Populationsof Primula vulgaris typically exhibit maximum frequency of about 80 per cent, and a floral dimorphism known as distyly (Darwin, appears to eliminate thrums prior to pins (although 1876; 1877). Approximately half the individuals in an exceptional population has been located con- distyled species have long styles and low anthers sisting solely of homostyles (Curtis and Curtis, (pins), the others having a short style and high 1985)). The long homostyle (homostyle hereafter) anthers (thrums). Both morphs are self-incompat- morph, which has a pin type gynoecium and a ible, and interfertile; thus distyly enforces out- thrum type androecium, is self-fertile, and has been crossing (Cahalan and Gliddon, 1985). The loci demonstrated to be largely self-fertilising in natural responsible for the dimorphism are rightly linked, populations (Crosby, 1959; Piper et a!., 1984; and are inherited as a supergene (Bateson and Curtis et a!., submitted for publication). Because Gregory, 1905); recombination within the super- homostyles have thrum type anthers, they compete gene occurs infrequently (Ernst, 1936a; b). with thrums for access to pin ovules, and although Usually there are two supergene "alleles", the in theory thrums can fertilise homostyles, this thrum form (dominant), and the pin form (reces- occurs infrequently because of the high rates of sive). Thrums are heterozygous at the supergene seif-fertilisation experienced by the homostyles. loci, and pins are homozygous, so the progeny of The appearance of this morph in populations of compatible matings are pins and thrums in a one this normally outcrossing species has been to one ratio. regarded as an example of the evolution of self- Despite low rates of recombination within the fertilisation (Fisher, 1941; Crosby, 1949; Dowrick, supergene, a recombinant homostyle form has 1956; Charlesworth and Charlesworth, 1979; Piper become established in Somerset populations of P. eta!., 1984, Curtis eta!., submitted for publication), although not without some controversy (Bodmer, tCurrentaddress and the one to which reprint requests should 1960; 1984; Crosby, 1960). be sent: Department of Biology, University of Chicago, 1103 A factor that has frequently been proposed E57th Street, Chicago, Illinois 60637, U.S.A. as playing a major role in the evolution of 208 J. G. PIPER, B. CHARLESWORTH AND D. CHARLESWORTH

self-fertilisationis reproductive assurance from February to May. Occasionally, in mild years, (reviewed by Jam (1976) and Lloyd (1980)). In a second flush of flowering occurs in late autumn environments where the transfer of pollen between (Clapham et a!. 1962). plants is restricted, due to poor pollinator service To obtain estimates of the fertility of self- in inhospitable environments (Hagerup, 1932; fertilising and outcrossing morphs of P. vulgaris, 1951; Baker, 1959; Ghiselin, 1969; 1974), self- population censusing was performed in Somerset incompatible or unisexual individuals cannot pro- populations, some with and some without homo- duce large seed crops. In contrast, autogamous styles, throughout the flowering seasons of 1982 individuals can, provided that inbreeding and 1983. In 1984, a less rigorous attempt to assess depression is not severe enough to induce high the relative fertility of self-fertilising and outcross- rates of progeny loss (Charlesworth and ing morphs was undertaken. Different numbers of Charlesworth, 1979; Lloyd, 1979; 1980). populations were censussed in each season, so that In 1984 (Piper eta!.,1984) we presented an 13 populations were studied in all over a 3 year outline of two factors involved in the evolution of period, several more than once. self-fertilisation (the rate of self-fertilisation, and In 1982, five populations (four with homo- the relative fertility of the self-fertile form), in styles) were visited at four to eleven day intervals Somerset populations of P. vulgaris. We now pro- from mid March to the end of May. On each visit, pose to describe our results on relative fertility the number of flowers, seed capsules, and the more thoroughly, and present additional data from number of flowers that failed to set seed were more populations, our primary aim being to recorded for each plant in a sample of the morphs explore further the role of reproductive assurance represented at the populations studied. This per- in the evolution of self-fertilisation. This was mitted the establishment of the total numbers of investigated by an assessment of the reproductive flowers and seed capsules produced by the three success of self-fertilising (homostyle) and out- morphs during the flowering season. After flower- crossing (pin and thrum) morphs in Somerset ing several naturally pollinated seed capsules per populations of P. vulgaris. plant were collected, and the number of seeds each Factors other than reproductive assurance can contained was determined. As seed capsule pro- affect the relative fertility of co-occurring, self- duction and the mean numbers of seeds per capsule fertilising and outcrossing morphs of the same were known for all individuals studied, total seed species. These factors include: differences in output per individual could be estimated. sexual resource allocation (Charlesworth and In 1983, a similar protocol to that followed in Charlesworth, 1981); differences in flower produc- 1982 was adopted, except that ten populations tion (Baker, 1965; Primack, 1978; Colosi and (seven with homostyles) were censussed at 11 to Cavers, 1984); and the expression of inbreeding 17-day intervals from mid March to the end of depression via seed abortion (Brink and Cooper, May. In addition, individual flowers (up to six per 1947; Rowlands, 1960; Link, 1961; Sayers and plant) were labelled on all plants at the start, in Murphy, 1966; Sorenson, 1969; Koski, 1971; the middle, and towards the end of the flowering Franklin, 1972; James, 1979) or reduced seed mass season, and their fates (i.e.,whetherthey did or (Darwin, 1876; Schaal and Leverich, 1984). An did not produce seed capsules) recorded. When attempt was made to establish the impact of these flower production among morphs does not differ, factors on the relative fertility of pin, thrum, and estimates of seed capsule production obtained by homostyle morphs of P. vulgaris, in addition to this method are equivalent to estimates of seed any effects of reproductive assurance. Differential capsule production on a per plant basis, though grazing of the flowers and capsules could affect formally they represent estimates of seed capsule the fecundity of the various morphs. This will be production per flower. Once again, estimates of the subject of a forthcoming publication. whole plant fertility for all the morphs were obtained. In 1984, six populations (three with homo- MATERIALSAND METHODS styles) were studied. No attempt was made to establish the floral output or total seed production (I) Population censusing for each individual. Instead, flowers were labelled Primulavulgaris. Huds is a perennial herbaceous at the peak of the flowering season, and those that species native to, and distributed throughout, the had set seed by the end of the season were col- British Isles. It has a basal rosette of leaves, and lected, and the number of seeds contained in each produces yellow flowers in a successional fashion capsule was established. BREEDING SYSTEM EVOLUTION IN PRIMULA VULGARIS 209

A map showing the locations of the popula- morphs of P. vulgaris was therefore assessed by tions, and frequencies of the morphs is presented comparing pollen grain production per anther by in fig. 1. thrums and homostyles. Two populations were chosen, one with a low homostyle frequency (ii)Reproductive assurance (Wanstrow 1), and one with a high homostyle frequency (Postlebury). Undehisced anthers from Todetermine if differences in pollen flow between 20 different individuals were collected from individuals could account for any differences in homostyles at both populations, and from thrums fertility among outcrossing and self-fertilising at Wanstrow 1. They were bisected, air dried, and morphs of P. vulgaris, one flower per pin and thrum crushed on a glass slide. The pollen grains were plant at all the populations studied in all seasons then spread over the slide surface and counted was pollinated by hand with compatible pollen. under a compound microscope. To assess invest- This was not done with homostyles; they receive ment made by outcrossing and self-fertilising sufficient pollen to achieve good seed set (Piper et morphs of P. vulgaris in female function, the ovule a!., 1984). The artificially pollinated capsules were number per ovary for 30 individuals of each morph collected after flowering, and the number of seeds at the populations studied in 1982 was determined. each contained was determined. Relative seed numbers and seed weights for the three morphs were also estimated. (iii)Sexual resource a/location Thrumtype anthers (i.e., those of thrums and (iv)Inbreeding depression homostyles) contain larger and less numerous pol- Toseek evidence for inbreeding depression in the len grains than pin type anthers; investment made progeny of homostyles in terms of abortion or in male function by outcrossing and seif-fertilising reduced seed mass, the numbers of seeds in

FROME

SHEPTON MALLET P wI INSET 1SEE BI P wB I Km

Figure 1 Map showing location and morph frequencies of the populations of Primulavulgaris studied.P: Postlebury, CL: Cloford, WI: Wanstrow 1, BW: Batcombe Wood, W3: Wanstrow 3, 82: Batcombe 2, E2: Eastcombe 2, El: Eastcombe 1, BI: Batcombe 1, W: Wyke Champflower, B: Bruton, C: Cogley. 210 J. G. PIPER. B. CHARLESWORTH AND D. CHARLESWORTH capsules of naturally pollinated flowers of out- In contrast to flower production, variation in crossing and self-fertilising morphs were counted, seed capsule production between the self- and known numbers of seeds of each morph were fertilising and outcrossing morphs over the three weighed on a Satorius model 1201 MP2 analytical years of study was very obvious. The seed capsule top pan balance to obtain a value of mean seed production data in table 1 reveals that there was mass for each morph. spatial variation in this index of fertility in 1982. At the two high frequency homostyle populations (Cloford and Postlebury), homostyles produced (v)Statistical analysis significantly more seed capsules than the outcrossing morphs, but at the low frequency homostyle Themean total number of flowers produced in a populations (Wanstrow I and Wyke) significant season, the mean number of seeds produced by differences were not observed. flowers that were naturally or artificially polli- A comparison of the seed capsule production nated, and the mean seed weights, for each morph data in tables 2 and 3 illustrates that there was in any one population were compared by one way temporal variation as well as spatial variation in analysis of variance, as were the mean numbers of seed capsule production of pins and thrums rela- pollen grains per anther, and the mean numbers tive to homostyles. In 1983 there was a tendency of ovules per ovary for each population. Non for homostyles to produce more seed capsules per orthogonal comparisons among means were made plant than pins and thrums. At four of the seven using the Tukey-Kramer method (Sokal and populations studied where homostyles and the out- Rohlf, 1981). The proportions of labelled flowers crossing morphs co-occurred (Cogley, Wyke, per morph that produced seed capsules (in 1983 Wanstrow 3, and Cloford), homostyles produced and 1984) were compared at each population by significantly more seed capsules per plant, an G tests of independence (Sokal and Rohlf, 1981.) observation confirmed by the censusing and the flower labelling data. At two of the remaining three populations (Wanstrow 2, and Bruton) the differences were not significant. However, at these RESULTS two poulations the outcrossing morphs produced significantly more flowers per plant, thus homo- (i) Flower and seed capsule production styles did produce more seed capsules per flower, if not more seed capsules per plant. Therefore, in Population censusing techniques employed in 1982 1983 homostyles tended to experience better seed and 1983 enabled the calculation of the mean total capsule production than pins and thrums. number of flowers, and the mean number of seed In 1984 this trend was not observed; at the capsules produced by each morph represented at three populations where homostyles were rep- the populations studied. These data are presented resented (Cogley, Bruton, and Postlebury) seed in tables 1 and 2. The results of the flower labelling capsule production among morphs did not differ. technique, adopted in 1983 and 1984 in order to These observations suggest that there were fluctu- assess the fates of individual flowers, are presented ations in pollinator services from year to year, and in tables 2 and 3. this theme is considered furtlier below. Examination of the data presented in tables 1 Analysis of seed capsule production by the and 2 suggests that there was not a consistent trend three morphs in the populations studied in 1982 in terms of the number of flowers produced in a and 1983 revealed another trend. The flower label- season by the three morphs of P. vulgaris. At ling data presented in table 2 show that in all Wanstrow I in 1982, thrums produced significantly populations (except Wyke and Cloford) where more flowers than homostyles, and at Wanstrow 2 pins, thrums and homostyles were represented, and Bruton in 1983 homostyles produced sig- pins matured more seed capsules per flower than nificantly fewer flowers than the outcrossing thrums. Population censusing in 1982 (table 1) also morphs in these populations. At all the other popu- showed this trend at Cloford. (It is probable that lations studied in 1982 and 1983 (except Cloford this trend was not observed at Cloford in 1983 in 1982, where homostyles produced significantly because of extremely high levels of predation. more flowers than pins and thrums) significant (Piper, 1984).) That pin seed capsule production differences among morphs were not observed. exceeds that of thrums where homostyles are pres- Clearly there is not an overall tendency for homo- ent suggests one cause of the elimination of thrums styles to produce fewer flowers than pins and prior to pins when homostyles are increasing in thrums. frea uencv. BREEDING SYSTEM EVOLUTION IN PRIMULA VULGAR/S 211

Table1 Fertility components, with their standard errors for pins, thrums, and homostyles at the populations studied in 1982

Mean seeds per capsule

Flowers Seed capsules Natural Artificial Seeds per Number Population Morph per plant per plant pollination pollination plant of plants

Batcombe 1 P 178±13 95±09 492±32 479±31 480±60 17 T 174±23 11•3±15 432±26 441±29 475±50 20 Wanstrow I P 36•7±33 148±26 454±36 44•9±41 647±122 17 T 44,943T 16•1+22 470±40 475±36 777±113 21 H 268±34 136±23 58.7±2.5** — 805±142 12 Wyke P 76±08 45±05 422± 18 560±471: 213±21 24 T 112±14 4•9±0•6 441±23 557±391: 238±33 26 H 74±0.6 5•0±05 52.3±2.4* — 255±29 27 Cloford P 129±13 79±1•1" 356±41 427±531: 3I6±S8 28 T 128±09 46±06 232±34 421±531: 143±21 15 H 151±10* 116±09* 45.0±2.0** — 513±49** 38 Postlebury P l34±09 67+06 443±29 566±361: 315±61 46 H 138± 10 8.8±0.8* 461± 17 408±54 26

TFOr this character, thrums greater than homostyles (p

Table 2 Components of fertility for pins, thrums, and homostyles at the populations studied in 1983. Values in the first five columns are presented with their standard errors. Numbers in brackets refer to the number of flowers that were labelled at each population.

Mean seeds per capsule % offlowers Flowers Seed capsules Natural Artificial Seeds per labelled Number Population Morph per plant per plant polination pollination per plant set seed of plants

Batcombe I P 122±12 57±11" 184±35 449±481: 154±41 67(92) 35 T 119± 1.1 3•3±06 I94±48 520±591: 87±25 31(108) 28 Batcombe 2 P l16±09 36±07 160±27 387±43t 82±24 32(92) 51 T 99±09 32±0.6 257±43 426±481: 123±31 56(95) 35 Batcombe P 118±12 4•3±O•6 182±26 447±441: 117±22 27(119) 50 Wood T 124±10 47±06 162±31 497±411: 107±21 24034) 49 Wanstrow 2 P 138±13 55±08 126±25 474±491: lI2±28' 12(91)" 36 T 142± 12 45±08 89±36 358±731: 40±19 3(134) 22 H 80±085•7±08 48.9±37** 316±53' 56(41)** 11 Cogley P 109±08 56±06 258±26 363±361: 171±24 35(j74)" 46 T 116±09 43±06 173±29 397±271: 114±26 14(209) 46 H 113±11 8.2±1.0* 42.9±3.2** 415±68' 60(134)** 36 Wyke P 108±15 45±07 242±33 491±411: 144±30 11(153) 44 T 120±12 53±07 239±30 458±511: 144±26 10(219) 42 H 98±08 7.0±0.6* 43.l±2.3** 365±45' 52(149)** 45 Wanstrow 3 P 116±10 62±07 183±29 46•4±4•3 162±36" 31(109)" 15 T 138±16 54±11 35±2•4 445±491: 19±8 5(42) 30 H 108±08 7.8±0.8* 42.9±3.3** 3744** 59(134)** 43 Cloford P 74±07 10±03 58±29 — 8±4 17(53) 40 T l00±09 08±03 66±30 — 11±7 7(111) 22 H 93±09 1.8±0.2* 19.2±35** 57± 13* 17(105) 30 Bruton P 170± I 8 9714 410± 25 499221: 35857 39(113) 44 H 133±15 81±10 53.1±2.1** — 368±57 37068) 49 Postlebury P 89±06 40±04 272±33 494±311: 146±22 27(130) 46 H 91 48±06 34•7±2•6 — 210±33 24017) 49

§ Forthis character, homostyles less than pins and thrums (p

Table 3Fertility components of pins, thrums, and homostyles at the populations studied in 1984. Values in the first two columns are presented with their standard errors

Mean seeds per capsule

. Number of Natural Artificial Number of % of flowers flowers Population Morph pollination pollination plants set seed labelled

Batcombe Wood P 375±38 496±46 21 55 58 T 42•1±4•1 466±27 21 48 60 Eastcombe 1 P 316±31 402±31 24 74 82 T 383±3•4 39•2±36 21 60 50 Eastcombe 2 P 321±38 425±31 30 60 33 T 237±41 267±44 20 88 25 Cogley P 329±3•3 39•9±34 24 80 55 T 408±3•4 46•3±27 34 85 61 H 44•2±39 — 36 95 43 Bruton P 445±26 499±24 37 85 61 H 406±26 — 35 80 68 Postlebury P 412±26 469±32 33 60 66 H 39•4±3•0 — 28 72 62

(ii) Seeds per capsule with natural and they do show that over the entire study area (with artificial pollination the exception of Postlebury) seed capsules produced by naturally pollinated homostyle flowers Tables1 to 3 also present the mean number of contained significantly more seeds than those of seeds per capsule for naturally and artificially pol- naturally pollinated co-occuring outcrossing linated flowers of the morphs in the populations morphs. Moreover, artificial pollination led to a studied in 1982, 1983, and 1984 respectively. These significant increase in seed number per capsule for data permit an assessment of the importance of pins and thrums. (In 1983 it was not possible to pollinator availability to the fertility of pins and make this comparison at Cloford due to high levels thrums, even in homostyleless populations. of capsule predation.) Clearly, in 1983 homostyles In three of the five populations studied in 1982 were almost universally more fertile than the out- seed capsules from naturally pollinated homo- crossing morphs in terms of this index of fertility, style flowers contained significantly more seeds and this must have been due to a paucity of pol- than those of naturally pollinated pin and thrum linators. Furthermore, that artificial pollination flowers (Wanstrow 1, Wyke, and Cloford). At the lead to an increase in seed production in pins and remaining homostyled population (Postlebury), thrums in all populations indicates that density homostyles did produce more seeds per capsule dependent factors did not account for differences than pins, but the difference was not significant. in seed capsule production among morphs in this Artificial pollination of pins and thrums led to an instance. increase in seed capsule fertility at three popula- The disparity in fertility between self-fertilising tions (Wyke, Cloford, and Postlebury) only. Thus and outcrossing morphs was less in 1984 than 1983 at Wanstrow 1 and Batcombe 1 pollinator availa- (table 3). Although none of the populations studied bility did not limit seed set in pins and thrums, in 1984 showed a significant response to artificial whereas it did in the other three populations, sup- pollination of pin and thrum flowers, in terms of porting the notion expressed above that there an increase in seed number per capsule, there was was spatial variation in pollinator availability. an obvious trend. At every population artificially That pollinator availability limited seed pro- pollinated flowers produced more seeds per cap- duction in three relatively high frequency homo- sule than naturally pollinated flowers. The proba- style populations, but not in two low frequency bility of artificial pollination causing an increase homostyle populations, prompted us to study more in seed production in all ten cases by chance alone populations in 1983 than in 1982, with a view to is approximately 0001 which is highly significant. examining the plausibility of a negative relation- This observation supports the view that the abund- ship between good pollinator service and low ance of pollinators limited seed set in pins and homostyle frequency. The data collected in 1983 thrums in 1984, and that the effect was smaller (table 2) do not confirm this relationship. However, than in 1982 and 1983. BREEDING SYSTEM EVOLUTION IN PRIMULA VULGAR/S 213

(iii) Whole plant fertility Postlebury homostyles produced 2472 197 pol- Tables1 and 2 also present the mean total seed len grains per anther. There is thus no evidence to support the notion of a reduction in resources output per plant for the morphs at the populations studied in 1982 and 1983 respectively. In 1982 devoted to male function in homostyles. Ornduff (1979) observed far more pollen grains in the homostyles produced significantly more seeds than anthers of thrums in a population of P. vulgaris at co-occurring outcrossing morphs only at Cloford. Beddlestead in Berkshire, though he used a At the remaining populations, homostyles did produce more seeds per plant, but the differences were different counting procedure to the one adopted here. Fortunately though, the ratio of pin pollen not significant. In 1983 homostyles experienced a production in pin and thrum anthers does not significantly higher fertility than co-occurring outcrossing morphs at all populations except two differ, whatever counting procedure is used (Piper (Bruton and Postlebury); it is likely that the in preparation) and as it is the ratios that we are concerned with here, differences in absolute values difference was nonsignificant at Bruton because are not important. pins produced many more flowers than homostyles (table 2). (b)Ovule production Table4 presents the mean Although it was not possible to obtain estimates number of ovules per ovary for the morphs at the of whole plant fertility in 1984 it is likely, in view populations studied in 1982. There were no sig- of the seeds per capsule, and the capsule produc- nificant differences among morphs, except at tion data, that homostyles, pins, and thrums had Wanstrow 1 where pin ovaries contained sig- essentially similar fertilities. nificantly fewer ovules than those of thrums and The whole plant fertility data reflect the tem- homostyles. Clearly, homostyles have not poral and spatial variation in pollinator availability experienced a reallocation of resources in favour inferred above. However, these data also show that of female function. in several populations where homostyles were present (Cloford in 1982, and Cogley, Wanstrow Table4Mean number of ovules per ovary, with standard 2, and Wanstrow 3 in 1983), pins produced sig- errors, for pins, thrums, and homostyles at the population nificantly more seeds per plant than thrums, pro- studied in 1982 viding more support for the notion that superior female fertility of pins, when homostyles are pres- Morph ent, prevents them from being eliminated as Population Pin Thrum Homostyle quickly as thrums. Batcombe 1 532± 18 564± 16 — Wanstrow 1 52.8±1.7* 618±18 598±21 (iv)Sexual resource allocation Wyke 590±16 560±22 543±18 Pollen Cloford 560±21 530±19 510±15 (a) Production Thetwo populations — chosen for study were the two most likely to show Postlebury 506±22 560± 18 evidence of a shift in sexual resources from male * Pinflowers produced fewer ovules per ovary than homostyles to female function in homostyles: at Wanstrow 1 and thrums (p

r 120 r

I 10

100

1982 1983 1984 Figure2 Half monthly rainfall in millimetres (histogram) and mean daily temperatures in °C (dotted line) for the study area in March, April, May, and June in 1982, 1983, and 1984. (Data provided by the Wessex Water Authority.) 216 J. G. PIPER. B. CHARLESWORTH AND D. CHARLESWORTH tial to play an important role in the evolution of BAKER, H. G. 1959. Reproductive methods as factors in speci- seif-fertilisation. It has also provided an explana- ation in flowering plants. Cold Spr. Harb. Symp. Quant. tion of another phenomenon observed in Somerset BioL, 24, 177—190. BAKER,H. G. 1965.Characteristics and modes of origin of populations of P. vulgaris. The population surveys weeds. In The genetics of colonising species. ed. H. G. Baker of Crosby (1949), and Curtis and Curtis (1985) on and G. L. Stebbins. Academic Press, New York. Somerset populations of P. vulgaris show that BARRETT, S. C. H. 1980. Sexual reproduction in Eichhornia thrums are eliminated prior to pins when homo- crassipes (water hyacinth). I. Fertility of clones from diverse regions. J. Appi. Ecol., 17, 101-112. styles are increasing in frequency. This relatively BATESON, W. AND GREGORY, R. p 1905. On the inheritance rapid elimination of thrums has been referred to of heterostylism in Primula. Proc. R. Soc. Lond. B., Biol. as "thrum decline" (Crosby, 1949). Sci. 76, 581—586. This study showed that, in several populations BAWA, K. S. 1974. Breeding systems of tree species of a lowland tropical community. Evolution., 28, 85—95. where pins, thrums, and homostyles co-occurred BODMER, W. F. 1960. The genetics of homostyly in populations pins were more seed fertile than thrums (tables 1 of Primula vulgaris. PhiL Trans. R. Soc. Lond. B. BioL Sci., and 2.) This disparity can be accounted for by the 242, 517-549. compatibility relationships of the various morphs. BODMER, W. F. 1984. Sex and generations of Primroses. Nature., Homostyles and thrums produce the same type of 310, 731. BRINK, R. A. AND COOPER, D. C. 1947. The endosperm in seed pollen, and so compete for access to pin ovules. development. Bot. Rev., 13, 426-542. Homostyles also have stigmas with the compatibil- CALAHAN, C. N. AND GLIDDON, C. 1985. Genetic neighbour- ity relationships of pins, but because they are hood sizes in Primula vulgaris. Heredity, 54, 65-70. almost exclusively self-fertilising, the quantity of CHARLESWORTH, D. AND CHARLESWORTH B. 1979. The thrum pollen that fertilises homostyles is negli- maintenance and bread down of distyly. Am. Nat., 114, 499—5 13. gible. Consequently, as homostyle frequency CHARLESWORTH, D. AND CHARLESWORTH, B. 1981. Alloca- increases the male fertility of thrums declines. The tion of resources to male and female function in herma- male fertility of pins also declines as thrums phrodites. Biol. J. Linn. Soc., 14, 57-74. become relatively less abundant, but their female CLAPHAM, A. R., TUTIN, R. G. AND WARBURG, E. F. 1962. Flora of the British Isles. 2nd edition. Cambridge University Press. fertility (relative to thrums) does not, because the COLOSI, J. C. AND CAvERS, P. B. 1984. Pollination affects per- frequency of thrum type pollen donors (thrums cent biomass allocated to reproduction in Silene vulgaris and homostyles) does not decline. The same is not (Bladder Campion). Am. Nat., 124, 299-306. true for thrums. As homostyles increase in CROSBY, J. L. 1949. Selection of an unfavourable gene complex. frequency, pins decrease, and as a result there is Evolution, 3, 121-230. CROSBY, J. L. 1959. Outcrossing on homostyle primroses. Hered- less pollen available for the fertilisation of thrums. ity, 13, 127—131. Therefore, an additional factor causing the elimi- CROSBY, J. L. 1960. The use of electronic computations in the nation of thrums is their poorer female fertility study of random fluctuations in rapidly evolving popula- (relative to pins) in the presence of homostyles. tions. Phil. Trans. R. Soc. Lond. B. BioL Sci., 242, 55 1-572. CURTIS, J. AND CURTIS, C. F. 1985. Homostyle primroses Finally, and perhaps most importantly, this revisited: variation in time and space. Heredity, 54,227—234. study demonstrates how a component of fitness DARWIN, C. 1876. Effects of cross and self ferlilisation in the (in this case fertility) can vary from population to vegetable kingdom. London. John Murray. population, and from season to season. In view of DARWIN, C. 1877. The different forms offlowers on plants of the this it can be seen that conclusions drawn from a same species. London. John Murray. DOWRICK, v. p ..1956.Heterostyly and homostyly in Primula few populations observed over a short time span obconica. Heredity, 10, 219-236. must be treated with extreme caution. Without long EISIKOWITCH, D. ANDGALIL,j.1971.Effect of wind on the term studies, it will be difficult to interpret models pollination of Pancratium maritimum L. (Amaryllidaceae) that attempt to chart the evolution of plant breed- by Hawkmoths (Lepidoptera: Sphingidae). J. Anim. Ecol., 40, 673-678. ing systems. ERNST, A. 1936a. Heterostylie-forschung. Versuche zur genetis- chen Analyse eines Organisationsund "Anpassungs" merk- Acknowledgements We thank Chris and Jill Curtis for provid- males. Z. Indukt. Abstammings-vererbungsl, 71, 156—230. ing accommodation during the field work phase of this project, ERNST, A. 19366. Weitere Untersuchungen zur Phananalyse and for furnishing us with their seemingly inexaustable local sum Fertilitatsproblem und zur Genetik heterostyler knowledge. This research was sponsored by an S.E.R.C. Quota Primein. II. Primula hortensis Wettstein. Arch Julius Klaus- award to J.G.P. Soft Vererbungsforsch. SoziaianthropoL Rassenhyg., ii, 1- 280. FISHER, R. A. 1941. Average excess and average effect of a gene REFERENCES substitution. Ann. Eugen., 11,53—63. FRANKLIN, E. C. 1972. Genetic load in loblolly pine. Am. Nat. ADAMS,M. U. 1967. Bases of yield component compensation 106, 262-265. in crop plants with special reference to the field bean, FREE, J. B. 1970. Insect pollination of crops. Academic Press, Phaseolus vulgaris. Crop Sci. 7 505-5 10. New York. BREEDING SYSTEM EVOLUTION IN PRIMULA VULGAR/S 217

GANDERS, F. R. 1975.Heterostyly, homostyly and fecundity in PRIMACK, R. B. 1978. Regulation of seed yield in Plantago, J. Amsinkia spectabilis (Boraginaceae). Madrono, 23, 56-62. Ecol., 66, 835—847. GHISELIN, M. T. 1969. The evolution of hermaphroditsm among PROCTOR, M. C. F. AND YEO, '.. 1973.The pollination of animals. Quart. Rev. Biol., 44, 189-208. flowers. Collins New Naturalist, London. GHISELIN,M. T. 1974. The economy of nature and the evolution ROWLANDS, D. ci. 1960. Fertility studies in field bean (Vicea of sex. University of California Press. faba L). I. Cross and self fertilisation. Heredity, 15, 161— HAGERUP, 0. 1932. On the pollination in the extremely hot air 173. at Timbuktu. Dansk. Bot. Ark, 8, 1-20. SAYERS, E. R. AND MURPHY, R. P. 1966. Seed set in Alfalfa as HAGERUP, ii 1950. Rain Pollination. D. KgL Danske. Vidensk related to pollen tube growth, fertilisation frequency, and Seisk Biol. Medd., 17,1-10. post fertilisation ovule abortion. Crop Sci., 6, 365—368. HAGERUP, o. 1951. Pollination in the Faroes—in spite of rain SCHAAL. B. A. AND LEVERICH, w. j.1984.Age-specific fitness and poverty in insects. D. Kg!. Danske. Vidensk. Selsk Biol. components in plants: genotype and phenotype. In: Popu- Medd., 18, 1-47. lation Biology and Evolution. Ed. K. Wohrmann, and V. HEINRICH, B. 1972. Temperature regulation in the bumblebee Loeschke. Springer-Verlag. Bombus vagans: a field study. Science, 175, 185—187. SCHEMSKE, D. w. 1977. Flowering phenology and seed set in .IAIN, S. K. 1976. The evolution of inbreeding in plants. Ann. Claytonia verginica (Pertulaceae). Bull. Torry. Bot. Club, Rev. Ecol. Syst., 7 469-495. 104, 254—263. JAMES, S. H. 1979. Chromosome numbers and genetic systems SCHEMSKE, D. W. 1980. Evolution of floral display in the orchid in the trigger plants of Western Australia (Styldium: Brassavola nodosa. Evolution. 34, 489-493. Stylidaea). Aust. J. Bot., 27,17—25. SCHEMSKE, D. W., WILLSON, M. F., MELAMPY, M. N., MILLER, JANZEN,D. H., DEVRIES,P., GLADSTONE, D. E., HIGGINS, C. J., VERNER, L., SCHEMSKE, K. M. AND BEST, L. .1978. M.L. AND LEWINSOHN, T. M.1980. Self and cross pollina- Flowering ecology of some spring woodland herbs. tion of Eucyclia cordigera (Orchidaceae) in Santa Rosa Ecology, 59, 351-366. National Park, Costa Rica. Biotropica, 12, 72-74. SOKAL, R. R. AND ROHLF, F. ..1981.Biometry: the principles KOSKI, v. 1971. Embryonic lethals of Picea abies, and Pinus and practice of statistics in biological research. 2nd edition, sylvestris. Comm. Inst. For. Fenn., 75, 1—30. W. H. Freeman. San Francisco. LANDE, R. AND SCHEMSKE, D. 1985. Evolution of self fertilisa- SOLERIG, 0. T. AND ROLLINS, R. C. 1977. The evolution of tion and inbreeding depression in plants. I. Genetic models. autogamy in species of the mustard genus Leavenworthia. Evolution. 39, 24-40. Evolution, 31, 265-281. LEVIN, D. A. 1972. Competition for pollinator service: a stimulus SORENSON, F. 1969. Embryonic genetic load in douglas fir for the evolution of autogamy. Evolution, 26,668-674. Pseudotsuga menziesii var menziesii. Am. Nat., 103, 389- LEVIN, D. A. ANDANDERSON, W. w. 1970.Competition for 398. pollinators between simultaneously flowering species. Am. STANTON, M. L. 1984. Developmental and genetic sources of Nat., 104, 455-467. seed weight variation in Raphanus raphinastrum L LINK, A..t. 1961.The morphological development of the seed (Brassicaceae). Am. J. Bot., 71, 1090-1098. of Pisum sativum var Alaska. Phytomorphology, 11, 79-83. WELLER, S. 0. 1980. Pollen flow and fecundity in populations LLOYD, D. G. 1979. Some selective forces affecting the frequency of Lithospermum carolinense. Am. J. Bot., 67, 1334-1341. of self fertilisation in angiosperms. Am. Nat., 113, 67—79. WELLS, H. 1979. Self-fertilisation advantageous or deleterious? LLOYD, D. G. 1980. Demographic factors and mating patterns Evolution, 33, 252-255. in angiosperms. In Demography and evolution in plant popu- WERNER, P. A. AND PLATT, w. j.1976.Ecological relatiOn- lations. ed. 0. T. Solbrig, Blackwell Scientific Publications. ships of co-occurring golden rods (Solidago: compositae). MIYAMOTO, s. 1960. Observations on the behaviour of Bombus Am. Nat., 110, 959-971. diversus Smith (Biological studies on Japanese bees 13) WILBUR, H. M. 1977. Propagule size, number and dispersion Insectes Sociaux, 7 39-56. pattern in Ambystoma, and Asciepias. Am. Nat., 111, 43- NAGYLAKI, T. 1976. A model for the evolution of self fertilisa- 68. tion and vegetative reproduction. J. Theor. Biol. 58, 55—58. WILLIS, J. C. AND BURKILL, H. 1895. Flowers and insects in ORNDUFF,R. 1979. Pollen flow in a population of Primula Great Britain. Part 1. Ann. Bot., 9, 227-273. vulgaris Huds. Bot. J. Linn. Soc., 78, 1—10. WILLIS, J. C. AND BURKILL, I. H. 1903. Flowers and insects in PETERSON, C., BROWN, J.H. AND KODRIC-BROWN, A. 1982. Great Britain. Part 2. Observations on the natural orders An experimental study of floral display and fruit set in Dipsaceae, Plumbaginaceae, Compositae, Umbelliferae, Chilopsis linearis. (Bignoniaceae). Qecologia, 55, 7—11. and Cornaceae, made in the Colva Mountains. Ann. Bot., PIPER, J. G. 1985. Breeding system evolution in Primula vulgaris. 17, 313—349. D.Phil. Thesis, Univ. of Sussex. WILSON, 0. F. 1929. Pollination of hardy fruits: insect visitors PIPER, J. 0., CHARLESWORTH, B. AND CHARLESWORTH, D. to fruit blossoms. Ann. Appl. Biol., 16, 602—629. 1984. A high rate of self-fertilisation and increased fertility WOODELL, S. R. i. 1960. What pollinates primulas? New Scien- in homostyle primroses. Nature, 310, 50-5 1. tist, 8, 568—571.