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Extreme Environments Select for Reproductive Assurance: Evidence from Evening Primroses (Oenothera)

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Extreme Environments Select for Reproductive Assurance: Evidence from Evening Primroses (Oenothera) New Phytologist Research Extreme environments select for reproductive assurance: evidence from evening primroses (Oenothera) Margaret E. K. Evans1,5, David J. Hearn2, Kathryn E. Theiss3, Karen Cranston4, Kent E. Holsinger3 and Michael J. Donoghue1 1Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06511, USA; 2Department of Biological Sciences, Towson University, 8000 York Road, Towson, MD 21252, USA; 3Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Road, U-3043, Storrs, CT 06269, USA; 4National Evolutionary Synthesis Center, 2024 W. Main Street, A200, Durham, NC 27705, USA; 5Present address: Origin, Structure, and Evolution of Biodiversity, UMR 7205, Museum National d’Histoire Naturelle, 16 rue Buffon, 75231 Paris, Cedex 05, France Summary • Author for correspondence: Competing evolutionary forces shape plant breeding systems (e.g. inbreeding Margaret E. K. Evans depression, reproductive assurance). Which of these forces prevails in a given Tel: +33 140793366 population or species is predicted to depend upon such factors as life history, eco- Email: [email protected] logical conditions, and geographical context. Here, we examined two such Received: 15 December 2010 predictions: that self-compatibility should be associated with the annual life history Accepted: 8 February 2011 or extreme climatic conditions. • We analyzed data from a clade of plants remarkable for variation in breeding system, life history and climatic conditions (Oenothera, sections Anogra and New Phytologist (2011) 191: 555–563 doi: 10.1111/j.1469-8137.2011.03697.x Kleinia, Onagraceae). We used a phylogenetic comparative approach and Bayesian or hybrid Bayesian tests to account for phylogenetic uncertainty. Geographic information system (GIS)-based climate data and ecological niche Key words: Baker’s law, climate, evolution, modeling allowed us to quantify climatic conditions. life history, Oenothera, plant breeding • Breeding system and reproductive life span are not correlated in Anogra and system, reproductive assurance, self-compatibility. Kleinia. Instead, self-compatibility is associated with the extremes of temperature in the coldest part of the year and precipitation in the driest part of the year. • In the 60 yr since this pattern was anticipated, this is the first demonstration of a relationship between the evolution of self-compatibility and climatic extremes. We discuss possible explanations for this pattern and possible implications with respect to anthropogenic climate change. self-incompatibility in seed plants (Weller et al., 1995; Igic Introduction & Kohn, 2001; Steinbachs & Holsinger, 2002; Igic et al., Puzzling over variation and evolution of plant breeding 2008), whereas change to self-compatibility is described as systems has occupied some of the greatest thinkers in the the most common evolutionary transition experienced by area of evolutionary biology (Darwin, 1876; Fisher, 1941; flowering plant lineages (Stebbins, 1974). On the other Dobzhansky, 1950; Stebbins, 1950, 1957). A central pattern hand, self-compatibility can be advantageous if it provides of interest is variation in inbreeding vs outbreeding, which is ‘reproductive assurance’: a plant that finds itself without thought to arise from competing evolutionary forces. On mates or pollinators may still be able to reproduce (Darwin, one hand, the negative fitness consequences of inbreeding 1876; Lloyd, 1979, 1992; Fausto et al., 2001; Weber & (known as inbreeding depression) favor outbreeding Goodwillie, 2009). These two selective factors, inbreeding (Nagylaki, 1976; Lande & Schemske, 1985; Charlesworth depression and reproductive assurance, are thought to be & Charlesworth, 1987). In many plants, self-incompatibility among the most important acting on plant breeding systems enforces outcrossing, so that self-fertilization, the most (Lloyd, 1979; Holsinger, 1996, 2000; Eckert et al., 2006). extreme form of inbreeding, is impossible. Phylogenetic Which of these competing forces wins out in shaping the analyses suggest that there have been relatively few origins of breeding system of a particular species or population is Ó 2011 The Authors New Phytologist (2011) 191: 555–563 555 New Phytologist Ó 2011 New Phytologist Trust www.newphytologist.com New 556 Research Phytologist context-dependent, including factors such as life history, tions (extreme temperatures, high latitudes and altitudes) ecological conditions, and geographical context. For exam- and selfing. ple, it is thought that selection for reproductive assurance Here we evaluate patterns of covariation and coevolution should be stronger in plants that have just one opportunity of reproductive life span (annual vs iteroparous perennial), to reproduce in their lifetime (annuals, monocarpic peren- breeding system, and climatic conditions in a clade of plants nials) compared with plants that have several chances to found in western North America: Oenothera sections reproduce (polycarpic perennials; Morgan et al., 1997; Anogra and Kleinia (Onagraceae). This group of 19 taxa is Morgan, 2001). Thus annuals should be more likely than remarkable for variation in climatic conditions, life history, perennials to evolve self-compatibility, whereas perennials and breeding system (Table 1). Some of the Anogra and should be more likely to retain self-incompatibility Kleinia taxa are found in low-elevation deserts of the south- (Stebbins, 1950; pp. 176–181). This prediction has been western USA, others in semiarid grasslands, and others in borne out in some surveys of plant breeding systems alpine meadows in the Rocky Mountain region (Wagner (Barrett et al., 1996) but not in others (Raven, 1979). et al., 2007; Evans et al., 2009). Ten of the Anogra and Ecological conditions are also thought to modify selec- Kleinia taxa are self-incompatible, four are polymorphic in tion on plant breeding systems. Insect pollinator abundance breeding system (either among or within populations), and can be low under cold conditions (i.e. at high elevations five are self-compatible (Klein, 1970; Raven, 1979; Theiss and latitudes), which might increase selection for reproduc- et al., 2010). In this same group, 10 are perennial, two are tive assurance in the plants found there (Moldenke, 1979; variable in life history, and seven are annual (Klein, 1970; Kalin Arroyo et al., 1985; Korner, 1999; but see Garcia- Evans et al., 2005; Wagner et al., 2007). This variation Camacho & Totland, 2009). Extremely arid conditions are makes the Anogra + Kleinia clade an excellent group in associated with variation in reproductive success (Beatley, which to evaluate coevolution of: breeding system and 1974; Kadmon & Schmida, 1990; Philippi, 1993; Clauss reproductive life span; and breeding system and climate. & Venable, 2000; Schemske & Bierzychudek, 2001), which We use a molecular phylogenetic comparative approach to may generate selection for reproductive assurance. Stebbins account for nonindependence of taxa. Because of the young (1950) generalized this by suggesting that extreme condi- age of the Anogra + Kleinia radiation (crown date within tions should favor the evolution of selfing: ‘selection in the last 1 million yr; Evans et al., 2009), there is consider- favor of self-fertilization is very likely to occur in all annuals able phylogenetic uncertainty (Fig. 1a), which we account and other short-lived plants living in deserts, alpine or arctic for using a sample from the posterior distribution of regions, or other extreme environments’. Lloyd (1992) Bayesian phylogenetic trees. We use geographic information made a similar association between environmental condi- system (GIS)-based climate data and ecological niche Table 1 Life history (LH), breeding system (BS), and climate data for all taxa in sections Anogra and Kleinia, Oenothera, Onagraceae Taxon Abbreviaton LH BS Pdry (cm) Pdry¼ (cm) Tcold¼ (°C) Tmin (°C) Oenothera wigginsii WIG A SC 0 0.23 13.28 5.31 O. deltoides ssp. cognata COG A ⁄ P SC 0.05 0.42 8.58 1.74 O. deltoides ssp. howellii HOW P SI 0.06 0.47 8.15 2.34 O. deltoides ssp. deltoides DELT A SI ⁄ SC 0.07 0.57 12.17 4.07 O. californica ssp. californica CAL P SI ⁄ SC 0.17 1.25 8.55 1.63 O. arizonica AZ A SC 0.26 1.26 12.45 4.14 O. californica ssp. eurekensis EUR P SI 0.52 2.10 4.03 )4.35 O. deltoides ssp. ambigua AMB A SI 0.62 2.98 4.52 )3.07 O. deltoides ssp. piperi PIP A SI 0.83 3.37 0.16 )7.09 O. californica ssp. avita AV P SI 0.84 3.48 2.51 )5.08 O. pallida ssp. runcinata RUNC P SI 0.89 3.41 1.96 )6.86 O. albicaulis ALB A SI 0.98 3.65 0.82 )7.80 O. pallida ssp. pallida PAL P SI ⁄ SC 1.08 4.16 )0.82 )7.87 O. pallida ssp. latifolia LAT P SI 1.11 3.85 )2.74 )11.46 O. engelmannii ENG A SI 1.13 4.07 5.24 )3.96 O. neomexicana NEO P SC 1.15 4.55 2.12 )6.66 O. nuttallii NUT P SC 1.19 4.07 )5.91 )13.98 O. pallida ssp. trichocalyx TRI P ⁄ B ⁄ A SI 1.22 4.16 )5.03 )13.26 O. coronopifolia COR P SI ⁄ SC 1.30 4.65 )2.64 )11.16 Life history states are annual (A), biennial (B), and perennial (P). Breeding system states are self-incompatible (SI) and self-compatible (SC). Climate variables are precipitation in the driest month (Pdry), precipitation in the driest quarter (Pdry¼), mean temperature in the coldest quarter (Tcold¼), and minimum temperature in the coldest month (Tmin). New Phytologist (2011) 191: 555–563 Ó 2011 The Authors www.newphytologist.com New Phytologist Ó 2011 New Phytologist Trust New Phytologist Research 557 (a) (b) Fig. 1 (a) Bayesian majority-rule consensus tree for Oenothera, sections Anogra and Kleinia (from the all-compat command in MrBayes). Posterior probabilities indicate the support for each node. Branch lengths are proportional to sequence change, in units of expected sequence change per site. (b) Maximum a posteriori tree with character mapping of life history (white, perennial; blue, annual) and breeding system (white, self-incompatible; red, self-compatible).
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