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0 Department of Biological Sciences University of Pittsburgh, Pittsburgh, Pennsylvania 15260 USA
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INTRODUCTION |
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 TOP INTRODUCTION LITERATURE CITED |
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In the 20 years since several treatises on gender and sexual dimorphism in plants (e.g., Lloyd and Webb, 1977
; Bawa, 1980
; Thomson and Barrett, 1981
; Givnish, 1982
; Lloyd, 1982
) rekindled an interest in these topics, hundreds of studies have been conducted. The majority of these were aimed at describing patterns of dimorphism, analyzing correlates of dioecy, and gathering empirical data relevant for testing theoretical models. The authors of GSDFP have made use of this wealth of data to formulate, and in some cases test, several novel hypotheses regarding gender evolution and its associated sexual dimorphism in life history, morphology, physiology, and biotic interactions. I am certain these hypotheses will stimulate new comparative research, especially in the more nascent areas of herbivore/pathogen impacts on sexual dimorphism, and of dimorphism in physiology and nonreproductive morphological traits. Nevertheless, the authors concur that now is the time to move beyond simple description of dimorphism and to focus on the quantitative variation in primary and secondary sexual traits within genders. Furthermore, they appropriately make an appeal for descriptions of the relationship between quantitative variation and fitness. Specifically, they argue that we need to measure natural selection on traits relevant to gender and dimorphism. These studies are crucial if we are to address fundamental questions regarding the evolution of sexual dimorphism, such as whether some traits (e.g., flower size, or photosynthetic rate) have stronger effects on fitness in one sex than the other, and whether different trait optima exist for males and females. The recent application of quantitative genetic theory to questions of natural selection in hermaphroditic and dioecious species (see Lande, 1980
; Meagher, 1992
; Morgan, 1992, 1994
) provides a rigorous framework for these studies (and is succinctly reviewed by Geber and Meagher, in Chapters 4 and 10, respectively). With reference to physiological and morphological traits, several authors (Chapter 6 and 7) go further by asserting that studies examining more integrated trait complexes (i.e., not single traits in isolation) are required if we are to truly understand the functional significance of sexual dimorphism. I would agree, and go a step further to suggest that studies on species with intermediate or transitionary breeding systems (e.g., gynodioecy) allow an analysis of selection on variation in both primary and secondary sexual characters and thus evaluation of how gender and sexual dimorphism coevolve. Moreover, it may be useful to extend the range of phenotypic variation (through artificial selection, hybridization or manipulation) so that one can view the entire selection surface. In addition, studies that address the role of selection through male fitness will fill a serious gap in our understanding. The authors of GSDFP are correct in asserting that this is an area ripe for future study, as few workers have used the quantitative genetic approach (but see Eckhart, 1993
; Kohorn, 1994
).
Possibly even more important is the message that much will be gained if we study the ecological context of evolution of dioecy and sexual dimorphism. For example, recently several independent lines of evidence (phylogenetic, within-species comparisons, and theoretical predictions) suggest a correlation between dioecy and dry or harsh habitats (reviewed in Ashman, 1999a
), a trend also noted by Darwin (1877): "we can however see that if a species were subject to unfavorable conditions ... the production of the male and female elements ... might prove too great a strain on its powers, and the separation of the sexes would then be highly beneficial" (p. 279), and "a very dry station apparently favors the presence of the female form" (p. 301). This renewed awareness of the context-dependent nature of the evolution of dioecy is particularly timely because a clear methodology exists for identifying causal environmental features. Specifically, the combination of phenotypic selection analyses and manipulation of the environmental context provides a very powerful means to identify the cause of selection (Wade and Kalisz, 1990
). In addition to habitat quality, pollen vectors may be manipulated to reveal a causal relationship between dioecy and certain modes of pollination. For example, experimental populations of plants can be screened with different gauged mesh to separate biotic from abiotic pollinator-mediated selection, or to separate selection mediated by different sized pollinators (e.g., Mazer and Meade, in press). The sex ratio is another major feature of the selective environment and is easily manipulable. For example, in gynodioecious species sex ratio can influence the level of pollen limitation in females (e.g., McCauley and Brock, 1998
), which in turn has implications for the evolution of dioecy (Maurice and Fleming, 1995
) and sex-specific selection on attractive traits (Wilson et al., 1994
).
The potential for selection on primary or secondary sexual characters to translate into an evolutionary response in gender or sexual dimorphism depends on the underlying genetics. Thus, an understanding of genetic architecture is needed in dioecious species, as well as those with related breeding systems (e.g., monoecy and gynodioecy). In Chapter 10, Meagher provides an elegant example of how quantitative genetic data can be used retrospectively to inform on past selection intensities on floral traits in Silene latifolia. Specifically, he combines data on the genetic variance-covariance matrices with putative historical levels of sexual dimorphism to estimate the selection gradients that would give rise to current levels of sexual dimorphism. Meagher, however, is careful to note the assumptions underlying these projection analyses, not the least of which is the putative ancestral phenotype. Prospective analyses are sorely needed to inform on how present day selection is contributing to dimorphism. Quantitative genetic studies in dimorphic plants are rare (Meagher, 1984, 1992
; Lyons, Miller, and Meagher, 1994
; Ashman, 1999b
), and I would urge attention be paid to the contribution of unequal heritabilities in the evolution of dimorphism (see Cheverud, Dow, and Leutenegger, 1985
), as well as the genetic correlation between the sex morphs. As both Meagher (Chapter 10) and Grant (Chapter 9) point out, another subject still in its infancy is the mechanism of quantitative genetic variation. That is, the underpinnings of genetic variation in gender and sexual dimorphism still await molecular dissection.
Since many chapters in GSDFP emphasize selection as a driver of sexual dimorphism, I think it is worth mentioning that the authors do warn against interpreting all examples of sexual dimorphism as examples of adaptive evolutionary responses to differing trait optima in the sexes. They point out, rightly so, that some differences may arise from inherent trade-offs experienced by the two sexes, i.e., limitations due to developmental or mechanical constraints. Again, multivariate selection gradient analyses followed by trait manipulation can be used to identify traits that are targets of selection (e.g., Campbell, Waser and Price, 1994
).
The phylogenetic perspective is also championed as a powerful avenue for resolving long-standing issues on several fronts. Sakai and Weller (Chapter 1) argue strongly that a phylogenetic perspective can aid in interpreting the significance of ecological and morphological correlates of dioecy. For example, they describe how phylogenetic data can be used to ascertain whether certain characters (or habitat shifts) spurred the evolution of dioecy (suggesting a causal association), or if the acquisition of dioecy permitted subsequent trait evolution (or habitat shift). Likewise, Webb (Chapter 3) suggests that phylogenetic information would allow more appropriate tests of the compensation hypothesis for female establishment and spread in gynodioecious species. He recommends comparisons between females of gynodioecious species with hermaphrodites of the ancestral species rather than conspecific hermaphrodites. Eckhart (Chapter 5) aptly suggests that some questions regarding the evolution of floral characters can only be addressed from a macroevolutionary perspective. For example, a phylogenetic approach could help evaluate competing explanations for why some dioecious species retain vestigial primary sexual organs (e.g., stamens in females) while others lack them. Specifically, a phylogenetic approach could determine whether interspecific differences in retention of vestigial organs arise from differences in the length of time since divergence from a hermaphroditic ancestor, or alternatively, from differences in ancestral breeding system (e.g., gynodioecy or monoecy). These are compelling arguments for the power of phylogenetic information, however this approach is not a panacea. Sakai and Weller (Chapter 1) acknowledge that while phylogenetic analyses have begun to shed light on some of the associations of dioecy with fleshy fruits and habitat shifts, the difficulties associated with creating phylogenetic trees (i.e., resolving order from tightly correlated traits, frequent transitions, or multiple parsimonious trees) have hindered fulfillment of their potential. Moreover, in the case of comparisons between females of gynodioecious species and putative ancestral hermaphrodites, an unmentioned assumption is it that there has been little change in the ancestral hermaphroditic lineage since splitting. More groups where dioecy has evolved from both monoecy and gynodioecy (such as the Solanum Eckhart mentions in Chapter 5) are needed to determine whether one route leads to complete dimorphism in primary sexual characters more often than the other. Studies that link microevolutionary forces mentioned above with macroevolutionary patterns that emerge from phylogenies will prove critical.
Theoretical models have played a central role in identifying factors important in the evolution of plant breeding systems and in guiding empirical research. Charlesworth (Chapter 2) and Geber (Chapter 4) see a continued role for theory in exploring the evolution of dioecy and sexual dimorphism. They provide reviews of the theory and then highlight issues that beg for further theoretical development. For example, the evidence that dioecy often evolves in harsh environments still requires a stronger connection with population genetic theory. The extent to which gender and sexual dimorphism coevolve is also an issue deserving of more attention. Such work is likely to lead to new connections between theory and patterns in dioecy and sexual dimorphism.
Individual chapters of GSDFP are rich in detailed case studies and reviews of our empirical knowledge base to date. And while not always exhaustive, they do provide the kind of depth necessary to give a new student a good grasp of the field, as well as an entré into the primary literature. However, there are some areas that get less attention than a reader would like. This reader would have appreciated more coverage of the role of nuclear-cytoplasmic gynodioecy in the transition to dioecy. Greater coverage would have allowed evaluation of the issues surrounding "stable" vs. "unstable gynodioecy" (e.g., Maurice et al., 1994
; Schultz, 1994
), and the role of this mode of sex determination in the evolution of sexual dimorphism. In addition, not all of the chapters on sexual dimorphism take advantage of studies conducted on species with breeding systems that are putative stepping stones to dioecy (e.g., gynodioecy and monoecy). These species can offer insights into the level of dimorphism that exists prior to the evolution of complete dioecy and the tradeoffs or constraints faced by hermaphrodites. Sometimes patterns in these breeding systems run counter to those found in dioecious species (see Chapter 5 on flower size dimorphism), and thus beg a more inclusive explanation. Likewise, a stronger call for empirical study of the conditions that favor conversion of hermaphrodites into males, and of the genetic trade-offs between male and female function in hermaphrodites is warranted. We have few such studies of these basic features of the "second step" in the evolution of dioecy (see Atlan et al., 1992
; Ashman, 1999a
). Lastly, despite the emphasis on phylogeny, the book lacked a figure of a phylogenetic tree with salient characters mapped on it; such a figure would have been very illustrative.
Overall, this book makes a compelling case that a cogent understanding of gender and sexual dimorphism is at our finger tips if we employ a multidisciplinary approach. These sentiments are consonant with those of other recent treatments of the evolution of plant mating strategies (e.g., Barrett, 1998
; Morgan and Schoen, 1997
). More specifically, by combining theory, phylogeny, and empirical study of ecology and genetics we can reach a new horizon in the study of plant gender. This is quite a challenge, but one that will be rewarding. I would recommend this book to practitioners and especially beginning graduate students, as it is sure to spark a flurry of well-directed research.
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FOOTNOTES |
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LITERATURE CITED |
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TOPINTRODUCTIONLITERATURE CITED |
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———. 1999b Quantitative genetics of floral traits in a gynodioecious wild strawberry Fragaria virginiana: implications for the independent evolution of female and hermaphrodite floral phenotypes. Heredity 83, in press.
Atlan, A., P. H. Gouyon, T. Fournial, D. Pomente, and D. Couvet. 1992 Sex allocation in an hermaphroditic plant: the case of gynodioecy in Thymus vulgaris L. Journal of Evolutionary Biology 5: 189–203. [CrossRef][ISI]
Barrett, S. C. H. 1998 The evolution of mating strategies in flowering plants. Trends in Plant Science 3: 335–341. [CrossRef][ISI]
Bawa, K.S. 1980 Evolution of dioecy in flowering plants. Annual Review of Ecological Systems 11: 15–39.
Campbell, D.R., N.M. Waser, and M.V. Price. 1994 Indirect selection of stigma position in Ipomopsis aggregata via a genetically correlated trait. Evolution 48: 55–68. [CrossRef][ISI]
Cheverud, J. M., M. M. Dow, and W. Leutenegger. 1985 The quantitative assessment of phylogenetic constraints in comparative analysis: Sexual dimorphism in body weight among primates. Evolution 39: 1335–1351. [CrossRef][ISI]
Darwin, C. 1877 The different forms of flowers on plants of the same species. University of Chicago Press, Chicago, Illinois, USA.
Eckhart, V. M. 1993 Do hermaphrodites of gynodioecious Phacelia linearis (Hydrophyllaceae) trade off seed production to attract pollinators? Biological Journal of the Linnean Society 50: 47–63.
Givnish, T. J. 1982 Outcrossing vs. ecological constraints in the evolution of dioecy. American Naturalist 119: 849–865. [CrossRef][ISI]
Kohorn, L. U. 1994 Shoot morphology and reproduction in jojoba: Advantages of sexual dimorphism. Ecology 75: 2384–2394. [CrossRef][ISI]
Lande, R. 1980 Sexual dimorphism, sexual selection and adaptation in polygenic characters. Evolution 34: 292–305. [CrossRef][ISI]
Lloyd, D. G. 1982 Selection of combined versus separate sexes in seed plants. American Naturalist 120: 571–585. [CrossRef][ISI]
———, and C. J. Webb. 1977 Secondary sex characters in plants. Botanical Review 43: 117–216.
Lyons, E. E., D. Miller, and T. R. Meagher. 1994 Evolutionary dynamics of sex ratio and gender dimorphism in Silene latifolia. I. Environmental effects. Journal of Heredity 85: 196–203.
Maurice, S., E. Belhassen, D. Couvet, and P. H. Gouyon. 1994 Evolution of dioecy: Can nuclear-cytoplasmic interactions select for maleness? Heredity 73: 346–354.
———, and T. H. Fleming. 1995 The effect of pollen limitation on plant reproductive systems and the maintenance of sexual polymorphisms. Oikos 74: 55–60. [CrossRef][ISI]
Mazer, S. J., and D. E. Meade. In press. Geographic variation in flower size in the wild radish: the potential role of pollinators in population differentiation. In T. A. Mousseau, B. Sinervo, and J. A. Endler [eds.], Adaptive genetic variation in the wild. Oxford University Press, Oxford, UK.
McCauley, D. E., and M. T. Brock. 1998 Frequency-dependent fitness in Silene vulgaris, a gynodioecious plant. Evolution 52: 30–36.
Meagher, T. R. 1984 Sexual dimorphism and ecological differentiation of male and female plants. Annals of the Missouri Botanical Garden 71: 254–264. [CrossRef][ISI]
———. 1992 The quantitative genetics of sexual dimorphism in Silene latifolia (Caryophyllaceae): I. Genetic variation. Evolution 46: 445–457. [CrossRef][ISI]
Morgan, M. T. 1992 The evolution of traits influencing male and female fertility in outcrossing plants. American Naturalist 139: 1022–1051. [CrossRef][ISI]
———. 1994 Models of sexual selection in hermaphrodites, especially plants. American Naturalist 144: S100–S125. [CrossRef][ISI]
———, and D. J. Schoen. 1997 The role of theory in an emerging new plant reproductive ecology. Trends in Ecology and Evolution 12: 231–234. [CrossRef]
Schultz, S. T. 1994 Nucleo-cytoplasmic male sterility and alternative routes to dioecy. Evolution 48: 1933–1945. [CrossRef][ISI]
Thomson, J. D., and S. C. H. Barrett. 1981 Selection for outcrossing, sexual selection, and the evolution of dioecy in plants. American Naturalist 118: 443–449. [CrossRef][ISI]
Wade, M. J., and S. Kalisz. 1990 The causes of natural selection. Evolution 44: 1947–1955. [CrossRef][ISI]
Wilson, P., J. D. Thomson, M. L. Stanton, and L. P. Rigney. 1994 Beyond floral Batemania: gender biases in selection for pollination success. American Naturalist 143: 283–296. [CrossRef][ISI]
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