Seasonal changes in physiological performance in wild Clarkia xantiana populations: Implications for the evolution of a compressed life cycle and self-fertilization

AJB Advance Article published on June 9, 2015, as 10.3732/ajb.1400557. The latest version is at http://www.amjbot.org/cgi/doi/10.3732/ajb.1400557 RESEARCH ARTICLE A M E R I C A N J O U R N A L O F B OTA N Y S EASONAL CHANGES IN PHYSIOLOGICAL PERFORMANCE IN WILD C LARKIA XANTIANA POPULATIONS : I MPLICATIONS FOR THE EVOLUTION OF A COMPRESSED LIFE CYCLE AND SELF - FERTILIZATION 1 L EAH S. D UDLEY 2,5 , A LISA A. H OVE 2 , S IMON K. E MMS 3 , A MY S. V ERHOEVEN 3 , AND S USAN J. M AZER 4 2 Warren Wilson College, P.O. Box 9000, Asheville, North Carolina 28815 USA; 3 University of St. Thomas, 2115 Summit Ave., St. Paul, Minnesota, USA 5105; and 4 University of California, Santa Barbara, Santa Barbara, California 93106 USA • Premise of the study: One explanation for the evolution of selfi ng, the drought escape hypothesis, proposes that self-fertilization may evolve under conditions of intensifying seasonal drought as part of a suite of traits that enable plants to accelerate the completion of their life cycle, thereby escaping late-season drought. Here, we test two fundamental assumptions of this hypoth- esis in Clarkia xantiana : (1) that a seasonal decline in precipitation causes an increase in drought stress and (2) that this results in changes in physiological performance, refl ecting these deteriorating conditions. • Methods: We examined seasonal and interannual variation in abiotic environmental conditions (estimated by ambient tempera- ture, relative humidity, predawn leaf water potentials, and carbon isotope ratios) and physiological traits (photosynthesis, conductance, transpiration, instantaneous water-use effi ciency, ascorbate peroxidase and glutathione reductase activities, quan- tum yield of photosystem II, PSII potential effi ciency) in fi eld populations of C. xantiana in 2009 and 2010. • Key results: In both years, plants experienced intensifying drought across the growing season. Gas exchange rates decreased over the growing season and were lower in 2009 (a relatively dry year) than in 2010, suggesting that the temporal changes from early to late spring were directly linked to the deteriorating environmental conditions. • Conclusions: Seasonal declines in transpiration rate may have increased survival by protecting plants from desiccation. Con- comitant declines in photosynthetic rate likely reduced the availability of resources for seed production late in the season. Thus, the physiological patterns observed are consistent with the conditions required for the drought escape hypothesis. Key words: California, Clarkia ; drought; gas exchange physiology; mating system evolution; Onagraceae; outcrossing; selfi ng. Evolutionary transitions in mating system within and be- tween angiosperm taxa are often associated with phenotypic evolution in phenological, life history, and fl oral traits, and the divergence between selfi ng and outcrossing sister taxa has been particularly well documented. Relative to their outcrossing rel- atives, predominantly selfi ng taxa often exhibit smaller fl owers, shorter styles, lower pollen production and pollen to ovule ra- tios, lower petal brightness and chroma, reduced herkogamy (i.e., greater proximity between anthers and stigmas), reduced dichogamy (i.e., more synchronous maturity of stigmas and an- thers), more rapid fl oral development, greater synchrony of fl ower production within individuals, earlier fl owering, shorter individual fl oral lifespan, or earlier senescence ( Cruden, 1977 ; 1 Manuscript received 23 December 2014; revision accepted 5 May 2015. The authors thank the National Science Foundation for support (grant OIS-0718227 to S.J.M. and L.S.D. and grant OIS-0718253 to S.K.E. and A.S.V.), and numerous UCSB undergraduates assisted in processing fi eld- collected samples. 5 Author for correspondence (e-mail: ldudley@warren-wilson.edu) doi:10.3732/ajb.1400557 Cruden and Lyon, 1985 ; Brunet, 1992 ; Eckhart and Geber, 1999 ; Dudley et al., 2007 ; Delesalle et al., 2008 ; Busch and Urban, 2011 ; Andersson, 2012 ; Button et al., 2012 ). The mechanisms that may contribute to the joint evolution of phenological, life history, and fl oral traits in selfi ng taxa relative to their outcrossing sister taxa have been described in detail elsewhere ( Rollins, 1963 ; Lloyd, 1979 ; Guerrant, 1989 ; Runions and Geber, 2000 ; Mazer et al., 2004 ; Goodwillie et al., 2006 ; Barrett et al., 2014 ). One proposed mechanism is that selfi ng evolves under conditions where selection favors geno- types with accelerated life cycles ( Lloyd, 1965 ; Moore and Lewis, 1965 ; Vasek and Sauer, 1971 ; Arroyo, 1973 ; Solbrig and Rollins, 1977 ; Guerrant, 1989 ; Aarssen, 2000 ; Mazer et al., 2004 ; Snell and Aarssen, 2005 ). Selfi ng can promote a more compressed life cycle because autogamous fl owers often have shorter fl oral lifespans and set seed more rapidly than the fl ow- ers of their outcrossing relatives do ( Armbruster et al., 2002 ; Eckhart et al., 2004 ; Dudley et al., 2007 ; Goodwillie et al., 2010 ; Runions and Geber, 2000 ; Mazer et al., 2004 ; Theiss et al., 2010 ; Wu et al., 2010; but see Hill et al., 1992 ). In addition, at the whole plant level, recent studies have found that fl owers are produced in more rapid succession in autogamous taxa than American Journal of Botany 102 ( 6 ): 1 – 11 , 2015 ; http://www.amjbot.org/ © 2015 Botanical Society of America Copyright 2015 by the Botanical Society of America