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The Ecological Genetics of Floral Traits Heredity (2006) 97, 86–87 & 2006 Nature Publishing Group All rights reserved 0018-067X/06 $30.00 www.nature.com/hdy NEWS AND COMMENTARY ...............................................................Adaptive evolution zygomorphs does not represent a long- term constraint on angiosperm evolu- The ecological genetics of floral tion. Studies that focus on lineages with both actinomorphic and zygomorphic traits species could be useful in resolving this contradiction between patterns of CM Caruso genetic variation within species and ........................................................... speciation within clades. Heredity (2006) 97, 86–87. doi:10.1038/sj.hdy.6800853; published online 31 May 2006 Finally, mean rg between flower size and number was not significantly dif- ferent from zero, which does not sup- loral traits have fascinated evolu- because evolution in response to natural port the hypothesis that the evolution of tionary biologists since Darwin selection is slower for species with floral displays is genetically constrained F published ‘The various contri- lower h2, self-pollinating angiosperm by a trade-off between the size and vances by which orchids are fertilized species will not be able to respond to number of flowers produced by a plant. by insects’ in 1862. Because flowers are novel selection pressures and conse- This is a significant result because the remarkably diverse and important for quently may have elevated extinction inverse relationship between flower size sexual reproduction in plants, floral rates. The evolution of selfing species and number is the type of resource traits are excellent subjects for studies from outcrossing ancestors is one of the allocation trade-off that underlies much of adaptive microevolution. In addition, most common evolutionary transitions of life history and sex allocation theory floral traits are unique among plant in angiosperms and, as such, Stebbins’ and is an assumption of many theore- traits because they can directly influ- hypothesis has dominated the field of tical models of floral evolution. Ashman ence pollinator-mediated reproductive plant evolutionary biology. Despite the and Majetic’s (2006) findings differ from isolation between species. Conse- importance of Stebbins’ hypothesis, three recent empirical studies (Caruso, quently, floral traits can provide a direct empirical data supporting the reduction 2004; Delph et al, 2004a, b), which found link between patterns of evolution with- of h2 in selfing species are scarce convincing evidence for negative r in species and rates of divergence (Takebayashi and Morrell, 2001), mak- g between flower size and number. These between species. ing the review a significant contribu- contrary results suggest that trade-offs A study recently published in Her- tion. Because self-compatible plant between flower size and number may edity (Ashman and Majetic, 2006) pro- species can have mixed mating systems be more apparent in some angiosperm vides the first review of empirical (both self-pollination and outcrossing), lineages than in others, but more esti- studies on the quantitative genetics of future studies should correlate the mates of genetic (or even phenotypic) floral traits. Their results indicate that realized selfing rate with h2 of floral floral evolution can be genetically con- traits to more definitively test whether correlations would be needed to test this strained and point to the ecological adaptive evolution is genetically con- hypothesis. conditions where these constraints will strained in selfing species. Ashman and Majetic (2006) tested an be more or less important. At the same The review also supports Berg’s impressive number of hypothesized time, this review highlights areas where (1960) hypothesis that traits of zygo- constraints on floral evolution, but the more research is needed. morphic (bilaterally symmetrical) flow- quality and quantity of studies included Quantitative genetics points to two ers with specialized pollinators are in the review suggest that their analyses possible constraints on adaptive evolu- more strongly correlated than traits of need to be interpreted with caution. 2 tion: first, natural selection on a trait actinomorphic (radially symmetrical) They analyzed h and rg because they will not result in adaptive evolutionary flowers with generalist pollinators. Berg were the most commonly reported change if there is little genetic variation predicted that floral integration (corre- parameters, but both are problematic. for that trait, and second, genetic covar- lated variation in floral traits) should be Heritabilities are ratios and thus can iation between traits can constrain their stronger in zygomorphic species be- reflect changes in genetic variation, adaptive evolution if there is an indirect cause it promotes precise pollination phenotypic variation, or both (Houle, response to natural selection via corre- by restricting which pollinators can visit 1992). Bivariate rg may under- or over- lated traits. Ashman and Majetic (2006) a flower, the direction from which they estimate constraints on evolution review estimates of genetic variation can approach, and their movement caused by indirect responses to natural and covariation for floral traits of 41 within the flower. Although widely selection (Blows and Hoffmann, 2005). species from 21 families, using herit- cited in studies of floral evolution, the In addition, the sample sizes for certain 2 abilities (h ) and genetic correlations (rg) empirical data for some of Berg’s (1960) hypotheses, particularly those related to as estimates of genetic variation and hypotheses are weak (Armbruster et al, sexually dimorphic species, were as low covariation, respectively. Their most 1999). However, Ashman and Majetic as N ¼ 3. Even though floral traits have interesting results address the effect of (2006) found that rg among floral traits been much more intensively studied mating system, floral symmetry, and of species with zygomorphic flowers than many other classes of plant traits, resource allocation on the quantitative were strong and positive relative to our ability to generalize about genetic genetics of floral traits. species with actinomorphic flowers, constraints on floral evolution is still Heritabilities for all classes of floral and suggest that high rg among floral limited by a lack of quality data. traits were lower in self-compatible traits may constrain the adaptive evolu- Although Ashman and Majetic’s species compared to self-incompatible tion of zygomorphs. Interestingly, (2006) review indicates that the evolu- ones, supporting Stebbins’ (1957) ‘evo- lineages with zygomorphic flowers are tion of floral traits can be genetically lutionary dead end’ hypothesis for why more speciose than those with actino- constrained, it also highlights the diffi- self-pollination is relatively uncommon morphic flowers (Sargent, 2004), imply- culty of relating these intraspecific con- in angiosperms. Stebbins argued that ing that high rg among floral traits of straints to patterns of angiosperm News and Commentary 87 speciation. In particular, this relation- CM Caruso is at the Department of Integrative Takebayashi N, Morrell PL (2001). Am J Bot 88: ship assumes that the same genes are Biology, University of Guelph, Guelph, Ontario, 1143–1150. responsible for intra- and interspecific Canada N1G 2W1. Further Reading differences in floral traits, an assump- tion that cannot be tested using Ashman TL (1999). Quantitative genetics of floral e-mail: [email protected] 2 traits in a gynodioecious wild strawberry estimates of h and rg. Fortunately, techniques such as quantitative trait Armbruster WS, Distilio VS, Tuxill JD, Flores TC, Fragaria virginiana: implications for indepen- Runk JLV (1999). Am J Bot 86: 39–55. dent evolution of female and hermaphrodite locus (QTL) mapping may make it Ashman TL, Majetic CJ (2006). Heredity 96: floral phenotypes. Heredity 83: 733–741. easier to relate the genes responsible 343–352. Elle E (1998). The quantitative genetics of sex for intra- and interspecific variation. For Berg RL (1960). Evolution 14: 171–180. allocation in the andromonoecious perennial, example, Hall et al (2006) found that Blows MW, Hoffmann AA (2005). Ecology 86: Solanum carolinense. Heredity 80: 481–488. 1371–1384. French GC, Ennos RA, Silverside AJ, Hollings- many of the QTL underlying variation Caruso CM (2004). Evolution 58: 732–740. worth PM (2004). The relationship between in floral traits within the wildflower Delph LF, Frey SM, Steven JC, Gehring JL (2004a). flower size, inbreeding coefficient and inferred Mimulus gutttus were also responsible Evol Dev 6: 438–448. selfing rate in British Euphrasia species. for differences in floral traits between Delph LF, Gehring JL, Frey FM, Arntz AM, Heredity 94: 44–51. Levri M (2004b). Evolution 58: 1936– Lendvai G, Levin DA (2003). Rapid response to Mimulus species. Ashman and Majetic’s 1946. artificial selection on flower size in Phlox. (2006) review should inspire more such Hall MC, Basten CJ, Willis JH (2006). Genetics 172: Heredity 90: 336–342. attempts to use modern molecular 1829–1844. Yoshioka Y, Iwata H, Ohsawa R, Ninomiya S techniques to dissect the genetics of Houle D (1992). Genetics 130: 195–204. (2005). Quantitative evaluation of the petal Sargent RD (2004). Philos Trans Roy Soc Lond Ser B shape variation in Primula sieboldii caused by floral traits and their implications for 271: 603–608. breeding process in the last 300 years. Heredity angiosperm evolution. Stebbins GL (1957). Am Nat 91: 337–354. 94: 657–663. Heredity.
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