ARE UNISEXUAL FLOWERS PRIMITIVE?

Transcription

1 New Phytol. (1986) 103, ARE UNISEXUAL FLOWERS PRIMITIVE? BY K. THOMPSON Department of Biological Sciences, Plymouth Polytechnic, Drake Circus, Plymouth PL4 8 A A, UK (Accepted 4 March 1986) SUMMARY Sporne's statistical evaluation of primitiveness in angiosperms has generated a good deal of controversy, mainly because his identification of unisexual flowers as primitive is at variance with most other interpretations of angiosperm evolution. The controversy can be resolved by taking account of the fact tbat (a) tbe bisexual and unisexual states are readily interchangeable and (b) there are good adaptive reasons for expecting unisexual flowers to be correlated with woodiness. Given tbat woodiness is Sporne's most important indicator of primitiveness, the apparent evaluation of unisexual flowers as primitive is seen to have an adaptive ratber than pbylogenetic basis. Key words: Angiosperms, evolution, unisexual flowers, primitive cbaracters, advancement index. INTRODUCTION Attempting to discover the nature of primitive angiosperms from the distribution of characters among living species has long been a popular pastime among botanists. The technique employed in these attempts, explicitly or otherwise, has been one of character correlation, building on a few characters of known and unambiguous primitiveness (e.g. vessel-less wood). The process is described succinctly by Cronquist (1968, p. 52). The quantity of data, concerning both new species and new characters, has grown to such an extent over the years, however, that the traditional subjective methods of weighing the evidence are no longer suflicient. It is against this background that Sporne (1949, 1976, 1980, 1982) has attempted to place the evaluation of primitiveness on an objective, statistical footing. There is almost complete agreement between Sporne's list of primitive characters and those produced by other authorities. It is a pity therefore that some writers (e.g. Cronquist, 1968; Stebbins, 1974) should have been dismissive of Sporne's ideas because they disagree with just one of his primitive characters, i.e. unisexual flowers. This paper attempts to reconcile these conflicting views. UNISEXUAL FLOWERS PRIMITIVE OR ADAPTIVE? Sporne has wisely resisted the temptation to introduce value judgements or weightings into his statistical assessment of primitiveness, preferring to let the data speak for themselves. This is a courageous decision, since most taxonomists evaluate the evidence in the light of many, chiefiy unspoken, assumptions about the 'value' of different characters (cf. Davis & Heywood, 1976, p. 38). Unisexual flowers emerge from Sporne's analysis as one of the more reliable indicators of primitiveness, a conclusion totally at variance with virtually every published X/86/ S03.00/ The New Phytologist

2 598 K. THOMPSON opinion on the subject. Cronquist (1968) has responded by simply ignoring Sporne almost completely '...his [Sporne's] analysis would suggest that the primitive flower was unisexual, whereas most botanists now believe it must have been bisexual'. Stebbins (1974), in contrast, has attempted to refute Sporne's conclusions. He suggests that the evaluation by Sporne of three other characters (woody habit, scalariform side walls and unstoried wood) as primitive and their positive association with unisexual flowers is a consequence of the expected association between the woody habit and wind pollination in temperate mesophytic floras. A fourth character, actinomorphic flowers, Stebbins also associates with anemophily, while a fifth, crassinucellate ovules, he associates with large seeds, another expected feature of woody plants. For Stebbins, then, Sporne's association between unisexual flowers and primitiveness is an artefact caused by the association between unisexual flowers and anemophily in temperate trees. This objection fails on at least two counts. First, although there is a sound ecological connection between unisexuality and anemophily in temperate trees, the same does not apply in the tropics. In the neotropics at least, most dioecious trees are pollinated not by wind but by small nonspecialist insects (Bawa & Opler, 1975; Bawa, 1980). Secondly, and more important, the temperate woody families which Stebbins probably had in mind (e.g. Aceraceae, Betulaceae, Fagaceae, Juglandaceae, Platanaceae, Salicaceae), and in which the combination of woodiness, anemophily and unisexuality is well developed, are not particularly primitive. The six families mentioned above have advancement indices (Sporne, 1980) ranging from 38 to 52, which is about average for the angiosperms as a whole. They do not, therefore, contribute to the statistical correlation between unisexual flowers and other primitive characters. This correlation arises from the large number of tropical and subtropical primitive families which are wholly (e.g. Schisandraceae) or partly (e.g. Stachyuraceae) unisexual. The great majority of these latter families, incidentally, are entomophilous. Another more cogent objection to Sporne's ideas has been proposed by Parkin (1951). Parkin has pointed out that, if we regard the primitive angiosperm flower as unisexual, it is strange that in bisexual flowers the stamens are always borne on the floral axis morphologically below the carpels. The reverse (or even mixed) condition appears not to have arisen. This suggests either that the selective pressure favouring such an arrangement is exceptionally strong, or that the transition from the unisexual to bisexual state occurred only once, very early in angiosperm evolution. The flrst possibility seems unlikely. The second is tantamount to admitting that the primitive angiosperms were bisexual, and certainly could not be responsible for Sporne's statistical evaluation of unisexual flowers as primitive. It is apparent, therefore, that there are numerous objections to regarding unisexual flowers as primitive, but that those who have attempted to explain away Sporne's undoubtedly genuine correlation (e.g. Stebbins, 1974) have not been entirely successful. One possible way out of the impasse is to examine the fossil record. Doyle & Hickey (1976), after a thorough study of North American leaf and pollen fossils from the mid-cretaceous Potomac group, conclude that the remains favour '...theories which assign this [primitive] position to the Magnoliales... '. They are, however, careful not to be too dogmatic about this opinion. More direct evidence comes from Cretaceous fossil flowers (Dilcher, 1979; Basinger & Dilcher, 1980). These authors show that while bisexual entomophilous flowers existed in the mid-cretaceous they were only one of at least three distinct flower

3 Are unisexual flowers primitive? 599 types, one of which was an apparently anemophilous, unisexual catkin. Dilcher (1979) suggests that the initial divergence between entomophilous and anemophilous types probably occurred very early in angiosperm evolution. At least for the present, theti, it seems that on the basis of the fossil record we cannot decide unambiguously whether the earliest primitive angiospei-ms were bisexual or unisexual. We must therefore return to a consideration of the characters of living angiosperms. An alternative approach is to consider these characters from an ecological, rather than a purely phylogenetic, viewpoint. First, it must be pointed out that unisexual flowers are a poor character from Sporne's point of view. As Stebbins (1974) has rightly pointed out, at least in primitive angiosperms, bisexuality vs unisexuality is a very readily reversible character. That this is the case is obvious from even a cursory examination of tbe families with low values of Sporne's advancement index. Those whose only acquaintance with the Magnoliaceae is growing them in a garden will no doubt be surprised to discover that the family is 'mixed', i.e. has unisexual and bisexual members. Those species with unisexual flowers are in a small minority and are clearly derived from bisexual ancestors. In the Schisandraceae, a very small family considered by some as part of the Magnoliaceae, the showy entomophilous male and female flowers are virtually identical and again seem to have a bisexual ancestor. In several otber primitive families (including, significantly, that with the joint lowest value of Sporne's index, the Aextoxicaceae) either the male or female flowers, or both, have rudimentary organs of the other sex. The derived nature of the unisexual condition in these latter families cannot be in doubt. In fact an examination of the 30 most primitive families, according to Sporne's index (up to a value of 35 inclusive), reveals perhaps only four or five families in which the unisexual condition is unambiguously primitive, in the sense of not being derived from bisexual ancestors. In contrast, 16 of tbese 30 families actually have unisexual members. Thus it seems that unisexual flowers are a poor character from an evolutionary point of view, in that the present state of the character reveals very little about its primitive, ancestral state. Note that if a significant proportion of the characters employed by Sporne proved to be as labile as sexuality, his whole approach could be invalidated. There is evidence that some characters have indeed changed state more than once during angiosperm evolution. For instance cellular endosperm, one of Sporne's advanced characters, is most common in the most advanced and the most primitive angiosperms, while supposedly primitive nuclear endosperm is most frequent in intermediate families (Dahlgren, 1975). Fortunately the majority of Sporne's primitive characters (e.g. woody habit, spiral phyllotaxy, presence of stipules, free petals) do not seem to be easily reversible in the way that unisexuality and perhaps some other characters are. Nevertheless the unisexual condition, derived or not, is correlated with an impressive list of other primitive characters. If unisexual flowers are not themselves primitive, how has this correlation arisen? The answer may lie in the correlation, pointed out by Lloyd (1982), between the frequency of separate sexes, and size and longevity of plants. The parallel correlation between self-incompatibility and woodiness suggests that the adaptive association is between longer generations and increased outcrossing (Lloyd, 1982). Note here that although Lloyd is talking specifically about dioecy, monoecy has a similar (though lesser) eflfect in increasing outbreeding. Lloyd proposes three possible causes of the relationship between long generations and selection for outcrossing. First, increased selfing among the more numerous flowers of larger plants. Second, more intense selection for

4 6oo K. THOMPSON heterosis as the ratio of juveniles to adults, and hence the level of competition, increases. Third, an increased benefit in longer-lived plants of recruiting new alleles at loci which protect plants against relatively short-lived predators and pathogens. The second two are likely to select for monoecy or dioecy, but the first clearly selects only for dioecy, or at least gynodioecy. Whatever the cause, however, there are clearly good reasons for expecting an adaptive correlation between unisexual flowers and longevity (and hence woodiness). Does this help to explain Sporne's findings? The woody habit is the single most important member of Sporne's list of primitive characters, in that it is involved in more statistically significant correlations than any other character. Indeed the 28 most primitive families (according to Sporne's index) are exclusively woody. In contrast, of the 28 most advanced families only three are wholly woody, and 15 are wholly herbaceous. The implication is clear; if there is an ecological correlation between unisexual flowers and woodiness, this alone would probably generate Sporne's statistical correlations involving unisexual tlowers and other primitive characters. There is selection for unisexual flowers in all long-lived woody plants, and primitive angiosperms are exclusively woody. This conclusion raises another problem with Sporne's whole approach. It has been argued here that unisexuality is an adaptive character, but of course it might also be argued that all characters are adaptive. Further, pairs or groups of adaptive character states may combine to form ecological 'strategies', in much the same way as unisexuality and woodiness. In some cases these strategies may be relatively obvious, such as the association of groups of floral character states with particular modes of pollination. In other cases the strategies may be extremely recondite. A hopeful sign is that, as mentioned previously, Sporne's list of primitive characters (with the obvious exception of unisexuality) is in good agreement with those derived from other sources, which suggests that the method is generally valid. Nevertheless, the distinct possibility that many of the character states are not ecologically independent must always be borne in mind. The above discussion suggests that the question of whether the ancestral angiosperms had unisexual or bisexual flowers is not amenable to solution by the statistical methods of Sporne (1949, 1976, 1980, 1982). The highly labile nature of unisexuality and the adaptive connection between this character and woodiness together account for Sporne's analysis being at odds with the generally held view that primitive angiosperms were bisexual. ACKNOWLEDGEMENTS I am grateful for the comments of R. A. Stevens and three referees on an earlier draft of this paper. REFERENCES BASINGER, J. F. & DlI.CIIER, D. L. (1980). Bisexual flowers from the mid-cretaceous of Nebraska. Botanicat Society of America, Miscettaneous Series, 158, 10. BAWA, K. S. (1980). Evolution of dioecy in flowering plants. Annuat Revie^v of Ecotogy and Systeinatics, 11, BAWA, K. S. & OPLER, P. A. (1975). Dioecism in tropical forest trees. Evotution, 29, CRONQUIST, A. (1968). The Evolution and Classification of Flowering Plants. Nelson, London. DAHLGREN, R. (1975). The distribution of characters within an angiosperm system. I. Some embryological characters. Botaniska Notiser, 128,

5 Are unisexual flowers primitive? 601 DAVIS, P. M. & HKYWOOD, V. H. (1976). Principles of Angiosperm Taxonoiny. Kriegt-r, New York. DILCHER, D. L. (1979). Early angiosperm reproduction: an introductory report. Review of Palaeohotany and Palynology, 27, DOYLE, J. A. & HICKEY, L. J. (1976). Pollen and leaves from the mid-cretaceous Potomae group and their bearing on early angiosperm evolution. In : Origin and Early Evolution of Angiosperms (Ed. C. B. Beck). pp. l.'! Columbia University Press, New York. LLOYD, D. G. (1982). Selection of combined versus separate sexes in seed plants. American Naturalist, 120, PARKIN, J. (1951). Tbe unisexual flower - a criticism. Pliytomorphology, 2, SPORNE, K. R. (1949). A new approach to the problem of tbe primitiveflower.new Phytologist, 48, SPORNE, K. R. (1976). Character correlations among angiosperms and tbe importance of fossil evidence in assessing their significance. In: Origin and Early Evolution of Angiosperms (Ed. by C. B. Beck), pp Columbia University Press, New York. SPORNE, K. R. (1980). A re-investigation of ebaracter correlations among dicotyledons. Nezv Phytotogist, 85, SPORNE, K. R. (1982). The advancement index vindicated. New Phytotogist, 91, STEBBINS, G. L. (1974). Flowering Ptants. Evolution above tlie Species Level. Harvard University Press, Cambridge, Massaehusetts.

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