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Divergent Mating Systems and Parental Conflict As a Barrier to Hybridization in Flowering Plants

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Divergent Mating Systems and Parental Conflict As a Barrier to Hybridization in Flowering Plants Divergent Mating Systems and Parental Conflict as a Barrier to Hybridization in Flowering Plants The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Brandvain, Yaniv and David Haig. 2005. Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants. American Naturalist 166(3): 330-338. Published Version http://dx.doi.org/10.1086/432036 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:2961254 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA vol. 166, no. 3 the american naturalist september 2005 ൴ Divergent Mating Systems and Parental Conflict as a Barrier to Hybridization in Flowering Plants Yaniv Brandvain1,* and David Haig2,† 1. College of the Atlantic, Bar Harbor, Maine 04609; During reproduction, males and females may be in conflict 2. Department of Organismic and Evolutionary Biology, Harvard over fertilization (Eberhard and Cordero 1995). After fer- University, Cambridge, Massachusetts 02138 tilization, parental conflicts continue because maternally Submitted October 31, 2004; Accepted April 22, 2005; and paternally inherited genes have different optima in Electronically published June 28, 2005 relation to maternal investment in offspring (Haig 2000). These conflicts are greatest in outcrossing populations, Online enhancement: appendix. while kin-based cooperation decreases conflict in inbred populations. Therefore, in outcrossing populations, strong paternal actions should be matched by equal maternal countermeasures. In inbreeding populations, these forces abstract: Parental conflicts can lead to antagonistic coevolution will be weaker but will be similarly balanced. Conse- of the sexes and of parental genomes. Within a population, the re- quently, crosses between plants of different mating systems sulting antagonistic effects should balance, but crosses between pop- will be unbalanced, with a strong force (the outcrosser) ulations can reveal conflict. Parental conflict is less intense in self- matched by a weak counterforce (the inbreeder). We call pollinating plants than in outcrossers because outcrossing plants are this the weak inbreeder/strong outbreeder (WISO) pollinated by multiple pollen donors unrelated to the seed parent, hypothesis. while a self-pollinating plant is primarily pollinated by one individual In relation to pollen-pistil interactions, “inbred” pollen (itself). Therefore, in crosses between plants with differing mating systems, outcrossing parents are expected to “overpower” selfing par- is predicted to mount a weak challenge to strong barriers ents. We call this the weak inbreeder/strong outbreeder (WISO) hy- in “outbred” styles, whereas outbred pollen should easily pothesis. Prezygotically, such overpowering can alter pollination suc- overcome the weak barriers of inbred styles. In relation to cess, and we argue that our hypothesis explains a common pattern seed development, paternally expressed genes are predicted of unilateral incompatibility, in which pollen from self-incompatible to cause rapid proliferation of the endosperm, while ma- populations fertilizes ovules of self-compatible individuals but the ternally expressed genes should inhibit endosperm growth reciprocal cross fails. A postzygotic manifestation of overpowering (Haig and Westoby 1991). The endosperm garners re- is aberrant seed development due to parent-of-origin effects such as genomic imprinting. We evaluate evidence for the WISO hypothesis sources from maternal tissue and nourishes the embryo by reviewing published accounts of crosses between plants of different and is the triploid product of the fertilization of the two mating systems. Many, but not all, of such reports support our hy- central cell nuclei of the megagametophyte. The strength pothesis. Since parental conflicts can perturb fertilization and de- of opposing parental forces is influenced by a population’s velopment, such conflicts may strengthen reproductive barriers be- mating system (Kondoh and Higashi 2000). Therefore, we tween populations, contributing to speciation. predict that hybrid seeds will show symptoms of paternal excess when the pollen parent is more outbred than the Keywords: weak inbreeder/strong outbreeder (WISO), genomic im- seed parent and maternal excess in the reciprocal cross printing, prezygotic, postzygotic, mating systems, speciation. (symptoms of maternal and paternal excess are discussed in “Postzygotic Effects on Seed Development” below). Both cases present barriers to hybridization and can thus contribute to speciation. * Present address: Department of Biology, Indiana University, Bloomington, Indiana 47405; e-mail: [email protected]. In the next two sections, we explain the relevance of † E-mail: [email protected]. the WISO to pollen-pistil interactions and seed develop- Am. Nat. 2005. Vol. 166, pp. 330–338. ᭧ 2005 by The University of Chicago. ment, respectively, and present predictions of our hy- 0003-0147/2005/16603-40718$15.00. All rights reserved. pothesis. Next, we summarize published information rel- Mating System, Conflict, and Hybridization 331 evant to the WISO hypothesis. Finally, we evaluate the Postzygotic Effects on Seed Development standing of this hypothesis. Seed development in many flowering plants depends on a correct ratio of maternal to paternal genomes (usually Pollen-Pistil Interactions 2 : 1) in the endosperm. Disruption of this ratio leads to abnormal development (Lin 1984; Haig and Westoby In most crosses between closely related self-incompatible 1991). Fertilization of a diploid by pollen from its own (SI) and self-compatible (SC) plants, SI pollen grows in autotetraploid derivative creates endosperm with two SC styles, but SC pollen is inhibited in SI styles (Lewis maternal and two paternal genomes and seed character- and Crowe 1958; de Nettancourt 1977). This pattern, la- ized by paternal excess. The reciprocal cross produces en- beled theSI # SC rule by Murfett et al. (1996), occurs in dosperm with four maternal genomes and one paternal taxa with gametophytic, sporophytic, and heteromorphic genome and seed characterized by maternal excess. In con- SI. In four exceptional cases, noted by Lewis and Crowe trast, self-fertilization of autotetraploids produces endo- (1958), in which SC pollen grew in SI styles, SC had orig- sperm with four maternal and two paternal genomes and inated only recently from SI. Thus, unilateral incompat- normally developed seed. ibility (UI) occurs in taxa with diverse SI mechanisms and The phenotypes of maternal and paternal excess are best appears to be a delayed response to changes in mating characterized for species in which the endosperm under- system. This suggests that theSI # SC rule is part of an goes free nuclear proliferation before it is cellularized. In adaptive response to changes in mating system, not a his- cases of maternal excess, the number of replications before torical accident or mechanistic necessity associated with cellularization is reduced, resulting in small, plump seeds. this change. With paternal excess, cellularization is delayed and often Pollen rejection inSI # SC crosses (seed parent first) fails altogether, resulting in seeds that are large but is a complex, multigenic process, but the S locus, which “empty” (Haig and Westoby 1991). Developmental failure is involved in SI, plays a role (Murfett et al. 1996; Bernacchi in crosses between some closely related diploid species and Tanksley 1997). The relative importance of the S locus, resembles failure of interploidy crosses (Sansome et al. however, is controversial (Hogenboom 1975). The obser- 1942; Stephens 1942; Reusch 1959a; Valentine and Woodell vations that there are exceptions to theSI # SC rule and 1963). This resemblance has been reconciled by assigning that the physiology, location, and timing of pollen tube genetic strengths to haploid genomes of different species arrest of UI is different than the SI reaction (Liedl et al. (Nishiyama and Yabuno 1978; Johnston et al. 1980; Kat- 1996) contribute to the controversy. siotis et al. 1995). Nonequivalent effects of maternal and We do not wish to add to this debate, but we suggest paternal genomes can be explained by the existence of that the WISO hypothesis provides an adaptive explana- imprinted genes (Haig and Westoby 1991), and imprinted tion for theSI # SC rule. In outcrossing species, pollen expression occurs in the endosperm (Vinkenoog et al. tubes are, for the most part, unrelated to the sporophytic 2003). Still, other mechanisms may explain some parent- tissues through which they grow and often are unrelated of-origin effects (Dilkes and Comai 2004; von Wangen- to the pollen tubes with which they “compete.” By con- heim and Peterson 2004). Regardless of mechanism, such trast, as self-pollination becomes more common, pollen differential expression allows for a manifestation of pa- tubes that compete for ovules approach genetic identity rental conflicts. Differences in levels of parental expression with each other and (except for ploidy) with the sporo- can act to prevent hybridization (Gutierrez-Marcos et al. phytic tissues through which they grow. Thus, the potential 2004), contributing to reproductive isolation and, ulti- for sexual conflicts is greatest in outcrossers, while the mately, speciation. benefit
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