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Rapid evolution of flowering time by an annual plant in response to a climate fluctuation Steven J Franks Sheina Sim and Arthur E Weis Department of Ecology and Evolutionary Biology University of California Irvine CA 92697 Edited 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 of many species and is expected to impose natural selection on ecologically important traits Droughts and other anticipated changes in precipitation may be particularly potent selective factors especially in arid regions Here we demonstrate the evolutionary response of an annual plant Brassica rapa to a recent climate fluctuation resulting in a multiyear drought Ancestral predrought genotypes were recovered from stored seed and raised under a set of common environments with descendant postdrought genotypes and with ancestor descendant hybrids As predicted the abbreviated growing seasons caused by drought led to the evolution of earlier onset of flowering Descendants bloomed earlier than ancestors advancing first flowering by 1 9 days in one study population and 8 6 days in another The intermediate flowering time of ancestor descendant hybrids supports an additive genetic basis for divergence Experiments confirmed that summer drought selected for early flowering that flowering time was heritable and that selection intensities in the field were more than sufficient to account for the observed evolutionary change Natural selection for drought escape thus appears to have caused adaptive evolution in just a few generations A systematic effort to collect and store propagules from suitable species would provide biologists with materials to detect and elucidate the genetic basis of further evolutionary shifts driven by climate change contemporary evolution global climate change life history theory local adaptation plant phenology M any species have shifted phenology the seasonal timing of reproduction and other life history events in response to ongoing climate change 1 3 For example a recent study reviewing flowering times FT in 461 plant species showed a trend of earlier flowering with climate warming 1 and another study showed shifts in plant flowering and bird and butterfly arrival dates in Mediterranean habitats 4 These shifts are largely attributed to rising temperatures but anticipated changes in precipitation 5 may also affect phenology especially in arid regions Observed shifts in phenology are due in part to direct effects of climate on physiological and developmental rates phenotypic plasticity However climate change can impose natural selection on phenology and thereby cause genetically based evolutionary shifts These shifts may occur rapidly providing important opportunities for the study of adaptive evolution in natural populations Abundant evidence has accumulated over the past several decades showing that natural selection can cause evolutionary change in just a few generations 6 7 Several cases of contemporary evolution implicate climate change as a selective agent using two general protocols The first compares contemporary and previous data on natural populations This approach has shown shifts over the past few decades in the frequencies of climate associated isozyme alleles and chromosome inversions across latitudinal gradients in Drosophila 8 10 Similarly pitcher plant mosquitoes from northern latitudes where growing seasons have lengthened now enter winter diapause at shorter photoperiods than they did in the 1970s while more southern 1278 1282 PNAS January 23 2007 vol 104 no 4 populations remain unchanged 11 The second protocol involves monitoring individuals in natural populations and inferring genetically based changes from the phenotypic resemblance between descendants and ancestors This method has demonstrated a genetic shift toward earlier parturition dates in red squirrels over the 1990s after increased artic spring temperatures 12 and showed shifts in beak morphology of Darwin s finches after drought changed food availability 13 These two general approaches provide convincing evidence for evolution by showing temporal changes in gene frequencies or phenotypes However by necessity these methods evaluate ancestral and descendant generations at different times and under potentially nonidentical conditions and so some important questions on the adaptive nature and genetic basis of these changes cannot be fully addressed We used a third experimental approach applicable to any species that can be stored in a dormant state This approach compares phenotypic and fitness values of ancestral descendant and ancestral descendant hybrid genotypes grown simultaneously under conditions that mimic the pre and postchange environments This method has several advantages Ancestors and descendants are reared together under the same controlled conditions so that phenotypic differences between ancestors and descendants can be partitioned into components due to genetic change and due to phenotypic plasticity By simulating pre and postchange conditions and measuring fitness in both environments it is possible to determine whether the descendant genotypes are better adapted to novel conditions or conversely that they have lost adaptation to past conditions The construction of hybrid lines provides information on the genetic basis and architecture of trait changes allowing phenotypic shifts to be partitioned into additive versus dominant gene effects 14 This approach thus combines the logic of the reciprocal transplant 15 and the line cross 14 experimental protocols which have explored evolutionary divergence between populations to investigate evolutionary changes within populations Previous studies have compared ancestors and descendants without hybrids to demonstrate the evolutionary response of Escherichia coli to elevated temperature in the laboratory 16 and in natural populations of Daphnia to study adaptation to water pollution 17 We used this general protocol to examine changes in phenology after drought We examined the evolutionary response of FT in field mustard Brassica rapa L Brassicaceae during a regional climate Author contributions S J F and A E W designed research S J F S S and A E W performed research 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 interest This article is a PNAS direct submission


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