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Seed Production from the Mixed Mating System of Chesapeake Bay (USA) Eelgrass (Zostera Marina; Zosteraceae)

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Seed Production from the Mixed Mating System of Chesapeake Bay (USA) Eelgrass (Zostera Marina; Zosteraceae) CORE Metadata, citation and similar papers at core.ac.uk Provided by College of William & Mary: W&M Publish W&M ScholarWorks VIMS Articles 2-2004 Seed production from the mixed mating system of Chesapeake Bay (USA) eelgrass (Zostera marina; Zosteraceae) JM Rhode Virginia Institute of Marine Science JE Duffy Virginia Institute of Marine Science Follow this and additional works at: https://scholarworks.wm.edu/vimsarticles Part of the Marine Biology Commons Recommended Citation Rhode, JM and Duffy, JE, "Seed production from the mixed mating system of Chesapeake Bay (USA) eelgrass (Zostera marina; Zosteraceae)" (2004). VIMS Articles. 1643. https://scholarworks.wm.edu/vimsarticles/1643 This Article is brought to you for free and open access by W&M ScholarWorks. It has been accepted for inclusion in VIMS Articles by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. American Journal of Botany 91(2): 192±197. 2004. SEED PRODUCTION FROM THE MIXED MATING SYSTEM OF CHESAPEAKE BAY (USA) EELGRASS (ZOSTERA MARINA;ZOSTERACEAE)1 JENNIFER M. RHODE2 AND J. EMMETT DUFFY College of William and Mary, School of Marine Science, P.O. Box 1346, Gloucester Point, Virginia 23062 USA In monoecious plants, gametes can be exchanged in three ways: among unrelated genets (outbreeding), with close relatives (in- breeding), or within individuals (geitonogamous sel®ng). These different mating systems may have consequences for population demography and ®tness. The experiment presented herein used arti®cial crosses to examine the mating system of Chesapeake Bay, Virginia, USA eelgrass (Zostera marina L; Zosteraceae), a bisexual submerged aquatic plant that can outbreed, inbreed, and self. Genetic data indicate severe heterozygosity de®ciencies and patchy genotype distribution in these beds, suggesting that plants therein reproduce primarily by vegetative propagation, autogamy, or geitonogamy. To clarify eelgrass reproductive strategies, ¯owers from three genetically and geographically distinct beds were hand-pollinated in outbred, inbred, and selfed matings. Fertilization success and seed production, life history stages which contribute greatly to the numeric maintenance of populations, were monitored. We found no evidence that inbreeding had negative consequences for seed production. On the contrary, selfed matings produced seeds signi®- cantly more frequently than outcrossed matings and produced signi®cantly larger numbers of seeds than either inbred or outbred matings. These results contrast with patterns for eelgrass in other regions but might be expected for similar populations in which pollen limitation or a short reproductive season renders sel®ng advantageous. Key words: inbreeding; mating system; outbreeding; reproductive assurance; seed production; self-fertilization; Zosteraceae; Zostera marina. Plant mating systems range from outbreeding among unre- hemisphere's most common temperate marine angiosperm lated individuals to inbreeding among relatives and self-fertil- (den Hartog, 1970), displays a full range of reproductive strat- ization (Shields, 1993; Waser, 1993b). The continuum of an- egies and is thus an ideal plant for mating system studies. It giosperm mating strategies corresponds to a range of conse- grows clonally, and populations usually consist of many ge- quences for the ecology and evolution of ¯owering plant pop- netically identical shoots (ramets) that form large intercon- ulations. Outbreeding tends to homogenize population genetic nected or fragmented genetic individuals (genets). Zostera ma- structure and can increase overall genetic diversity (Waser, rina is monoecious, with female and male ¯owers on a single 1993a). Conversely, outbreeding can result in the break-up of in¯orescence, so genetic exchange might occur within individ- multi-locus genotypes and disruption of local adaptation, lead- ual ramets as well as within and among populations (Ruck- ing to reduced offspring ®tness (outbreeding depression) (e.g., elshaus, 1995). Flowering shoots and the in¯orescences they Montalvo and Ellstrand, 2001). Though outbreeding depres- bear mature from the bottom up (acropetally), and ¯owers on sion has been demonstrated via arti®cial matings for several a single in¯orescence emerge asynchronously, with stigmas terrestrial plant species, it seems to occur less frequently than maturing ®rst (protogyny) and pollen released 48 h later (de inbreeding depression (reviewed in Waller [1993] and Waser Cock, 1980). Thus, while self-fertilization within eelgrass in- [1993a]). At the other extreme of the mating continuum, self- ¯orescences in nature is probably rare, ¯owering is not coor- fertilization maximizes the parent's genetic contribution to its dinated among ramets, so geitonogamy (self-fertilization offspring and avoids recombination with poorly adapted ge- among in¯orescences on different ramets of the same genet) notypes. However, offspring produced by selfed matings often probably occurs (Reusch, 2001). Vegetative expansion of eel- experience inbreeding depression, indicated by reduced het- grass patches is rapid (Olesen and Sand-Jensen, 1994a, b), erozygosity and the expression of deleterious mutations (re- viewed in Waller [1993] and Waser [1993a]). Self-fertilization seed production is unpredictable in both space and time (Sil- is rarely the most ®t plant mating strategy, but it provides berhorn et al., 1983; van Lent and Verschuure, 1995; Meling- reproductive assurance while retaining a mechanism for out- Lopez and Ibarra-Obando, 1999), and mortality of eelgrass breeding (Waser, 1993b). seeds (Fishman and Orth, 1996; Orth et al., 2000) and seed- Eelgrass (Zostera marina L.; Zosteraceae), the Northern lings (Hootsmans et al., 1987) can exceed 90%. Because eelgrass ¯owering tends towards protogyny, pre- vious research assumed that most seeds were produced by out- 1 Manuscript received 11 March 2003; revision accepted 11 September breeding (Setchell, 1929; de Cock, 1980; Phillips et al., 1983). 2003. The authors thank R. J. Orth and K. A. Moore for greenhouse space and Genetic and breeding studies of European and Washington, equipment; M. B. Cruzan, M. C. Harwell, A. P. Ramakrishnan, K. R. Reece, USA, populations demonstrated that self-fertilization is pos- and S. L. Williams for comments on this manuscript; and the National Science sible but occurs infrequently. Hand pollination produced some Foundation (pre-doctoral fellowship to J. M. R.), Virginia Institute of Marine inbred seeds (Cox et al., 1992; Ruckelshaus, 1995), and a mi- Science, and the College of William and Mary/School of Marine Science for crosatellite survey by Reusch (2001) indicated that many seeds funding. This is contribution # 2567 from the Virginia Institute of Marine Science. from two Baltic Sea populations were produced by geitono- 2 Current address: Department of Biology, Portland State University, P.O. gamy. However, most seedlings and adults in manipulated and Box 751 Portland, Oregon 97207 USA. E-mail: [email protected]. natural populations were produced by outcrossing (Ruckel- 192 February 2004] RHODE AND DUFFYÐSEED PRODUCTION IN EELGRASS 193 shaus, 1994; Reusch, 2000, 2001). Allozyme and molecular dividuals from three geographically, morphologically, and genetically differ- studies revealed high inbreeding coef®cients within many ent beds (Rhode, 2002): Allen's Island, Brown's Bay, and Broad Bay (Fig. beds, but the relative ®tness of offspring produced by geiton- 1). Allen's Island and Brown's Bay are geographically proximate and might ogamy or inbreeding was low compared to outbred progeny be expected to have regular propagule exchange, while Broad Bay is more (Ruckelshaus, 1995; Reusch, 2000, 2001). The geographic and isolated but has a much lower inbreeding coef®cient (FIS) (Rhode, 2002). ecological range of Zostera marina is vast (Phillips et al., Plants from Allen's Island and Broad Bay are signi®cantly longer and wider 1983), however, and eelgrass mating systems might vary with than those from Brown's Bay, but shoot density in Brown's Bay is signi®- environment or region. cantly higher than in the other two sites. Plants in Broad Bay are signi®cantly Eelgrass populations in Chesapeake Bay, USA, occupy the less inbred than the other two beds, but other estimates of genetic diversity southern limit of their biogeographic range, and they are dra- do not differ among the sites. In natural populations, seed production by Broad matically different from their counterparts in Europe and other Bay plants is signi®cantly lower than that from the other two beds (Rhode, 2002). parts of North America. In the Baltic Sea, a relatively stable In spring (April) 1998, 140 reproductive shoots were collected at haphazard environment, eelgrass clones are large and persistent (Reusch locations within each of the three sites. Each reproductive shoot was collected et al., 1999a, b; Reusch, 2000). Chesapeake Bay populations, with an attached vegetative shoot to provide a source of photosynthate for its conversely, are demographically dynamic, and their life cycle developing ¯owers and seeds. Distance between collection spots exceeded 2 includes summer defoliation and dieback (Orth and Moore, m to minimize resampling of single genets (as in Ruckelshaus, 1994). Shoots 1986). Clones seem to be much smaller, with beds less than 5 were transported to a greenhouse, where they were tagged to identify the site ha consisting of at least 12 genetic individuals (estimated from of origin. Each shoot was then planted in a 20
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