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Rapid evolution of flowering time

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Rapid evolution of flowering time by an annualplant in response to a climate fluctuationSteven J. Franks*, Sheina Sim, and Arthur E. WeisDepartment of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697Edited by Barbara A. Schaal, Washington University, St. Louis, MO, and approved November 30, 2006 (received for review September 22, 2006)Ongoing climate change has affected the ecological dynamics ofmany species and is expected to impose natural selection onecologically important traits. Droughts and other anticipatedchanges in precipitation may be particularly potent selective fac-tors, especially in arid regions. Here we demonstrate the evolu-tionary response of an annual plant, Brassica rapa, to a recentclimate fluctuation resulting in a multiyear drought. Ancestral(predrought) genotypes were recovered from stored seed andraised under a set of common environments with descendant(postdrought) genotypes and with ancestorⴛdescendant hybrids.As predicted, the abbreviated growing seasons caused by droughtled to the evolution of earlier onset of flowering. Descendantsbloomed earlier than ancestors, advancing first flowering by 1.9days in one study population and 8.6 days in another. The inter-mediate flowering time of ancestorⴛdescendant hybrids supportsan additive genetic basis for divergence. Experiments confirmedthat summer drought selected for early flowering, that floweringtime was heritable, and that selection intensities in the field weremore than sufficient to account for the observed evolutionarychange. Natural selection for drought escape thus appears to havecaused adaptive evolution in just a few generations. A systematiceffort to collect and store propagules from suitable species wouldprovide biologists with materials to detect and elucidate thegenetic basis of further evolutionary shifts driven by climatechange.contemporary evolution 兩 global climate change 兩 life history theory 兩local adaptation 兩 plant phenologyMany species have shifted phenology (the seasonal timing ofreproduction and other life history events) in response toongoing climate change (1–3). For example, a recent studyreviewing flowering times (FT) in 461 plant species showed atrend of earlier flowering with climate warming (1), and anotherstudy showed shifts in plant flowering and bird and butterflyarrival dates in Mediterranean habitats (4). These shifts arelargely attributed to rising temperatures, but anticipated changesin precipitation (5) may also affect phenology, especially in aridregions. Observed shifts in phenology are due in part to directeffects of climate on physiological and developmental rates(phenotypic plasticity). However, climate change can imposenatural selection on phenology and thereby cause geneticallybased evolutionary shifts. These shifts may occur rapidly, pro-viding important opportunities for the study of adaptive evolu-tion in natural populations.Abundant evidence has accumulated over the past severaldecades showing that natural selection can cause evolutionarychange in just a few generations (6, 7). Several cases of contem-porary evolution implicate climate change as a selective agent,using two general protocols. The first compares contemporaryand previous data on natural populations. This approach hasshown shifts over the past few decades in the frequencies ofclimate-associated isozyme alleles and chromosome inversionsacross latitudinal gradients in Drosophila (8–10). Similarly,pitcher plant mosquitoes from northern latitudes, where growingseasons have lengthened, now enter winter diapause at shorterphotoperiods than they did in the 1970s, while more southernpopulations remain unchanged (11). The second protocol in-volves monitoring individuals in natural populations and infer-ring genetically based changes from the phenotypic resemblancebetween descendants and ancestors. This method has demon-strated a genetic shift toward earlier parturition dates in redsquirrels over the 1990s after increased artic spring temperatures(12) and showed shifts in beak morphology of Darwin’s finchesafter drought changed food availability (13). These two generalapproaches provide convincing evidence for evolution by show-ing temporal changes in gene frequencies or phenotypes. How-ever, by necessity, these methods evaluate ancestral and descen-dant generations at different times and under potentiallynonidentical conditions, and so some important questions on theadaptive nature and genetic basis of these changes cannot be fullyaddressed.We used a third experimental approach applicable to anyspecies that can be stored in a dormant state. This approachcompares phenotypic and fitness values of ancestral, descendant,and ancestral⫻descendant hybrid genotypes grown simulta-neously under conditions that mimic the pre- and postchangeenvironments. This method has several advantages. Ancestorsand descendants are reared together under the same controlledconditions so that phenotypic differences between ancestors anddescendants can be partitioned into components due to geneticchange and due to phenotypic plasticity. By simulating pre- andpostchange conditions and measuring fitness in both environ-ments, it is possible to determine whether the descendantgenotypes are better adapted to novel conditions, or, conversely,that they have lost adaptation to past conditions. The construc-tion of hybrid lines provides information on the genetic basis andarchitecture of trait changes, allowing phenotypic shifts to bepartitioned into additive versus dominant gene effects (14). Thisapproach thus combines the logic of the reciprocal transplant(15) and the line cross (14) experimental protocols, which haveexplored evolutionary divergence between populations, to in-vestigate evolutionary changes within populations. Previousstudies have compared ancestors and descendants (withouthybrids) to demonstrate the evolutionary response of Escherichiacoli to elevated temperature in the laboratory (16) and in naturalpopulations of Daphnia to study adaptation to water pollution(17). We used this general protocol to examine changes inphenology after drought.We examined the evolutionary response of FT in field mus-tard, Brassica rapa L. (Brassicaceae), during a regional climateAuthor contributions: S.J.F. and A.E.W. designed research; S.J.F., S.S., and A.E.W. performedresearch; S.J.F., S.S., and A.E.W. analyzed data; and S.J.F. and A.E.W. wrote the paper.The authors declare no conflict of


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