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Home , Fitness (biology), Hybrid (biology)

Review fitness across time and habitats

Michael L. Arnold1 and Noland H. Martin2

1 Department of , University of Georgia, Athens, GA 30602, USA 2 Department of , Texas State University–San Marcos, San Marcos, TX 78666, USA

There has been considerable debate about the role of vation has been used to argue that genetic exchange via hybrids in the evolutionary process. One question has horizontal transfer (involving prokaryotic lineages) or involved the relative fitness of hybrid versus non-hybrid viral recombination can result in similar outcomes to those . For some, the assumption of lower hybrid obtained through (i.e. via natural fitness continues to be integral to their concept of hybridization [7]). Specifically, novel evolutionary lineages and . In contrast, numerous workers might arise that possess elevated fitness, relative to the have suggested that hybrid genotypes might demon- parental lineages, in novel environments. It would there- strate higher relative fitness under various environmen- fore seem important to broaden the discussion to include tal settings. Of particular importance in deciding viral and prokaryotic lineages. Second, in addition to the between these opposing hypotheses are long-term consideration of only , when the previous review analyses coupling ecological and genetic information. was published there was a lack of information that would Although currently rare, such analyses have provided a allow a fine-scale genotypic description of different test of the fitness of hybrid genotypes across gener- hybrids. The technical revolution of the last 15 years ations and habitats and their role in and has alleviated this deficiency by making possible the sim- speciation. Here we discuss examples of these analyses ultaneous analysis of numerous loci. Finally, fitness esti- applied to viruses, prokaryotes, and Darwin’s mates were generally based upon only one component (e.g. . survivorship), and these estimates were almost never derived from analyses across generations or habitats Hybrid fitness as a testable hypothesis (but see [8]). In their 1995 Trends in Ecology and review, In this article, we review recent examples from viral, Arnold and Hodges [1] argued that and prokaryotic and eukaryotic groups that have provided infor- hybrids could show reduced, equivalent or higher fitness mation on the relative fitness of hybrid genotypes. We will than their parents depending upon both their genotypic focus specifically on examples that highlight the fundamen- makeup and the environment in which they occurred. tally important role played by long-term investigations of These authors concluded that by environment hybrid fitness that span multiple generations and habitats, interactions would affect the fitness of hybrids just as they and which have a detailed genetic component. Together do nonhybrids. Though not a new idea [e.g. see 2–4], the these examples provide a definition of the genetic architec- suggestion that hybrids could possess higher fitness than ture of hybrid fitness and allow a test of models that predict ‘pure species’ genotypes ran counter to the prevailing uniformly low or, alternatively, variable hybrid fitness. conceptual framework. This framework rested firmly on This, in turn, provides the opportunity to highlight the the related hypotheses that speciation must occur under potential role of genetic exchange in adaptive evolution. allopatric conditions, and that lineages were not ‘good In particular, the findings discussed provide tests for adap- biological species’ if they exchanged with other tive trait and adaptive lineage formation. species (see [5] for a review). These assumptions resulted in the conclusion that hybridization would almost never of recombinant viruses and bacteria occur during speciation (because species had to arise in Because of the implications for human health, pathogenic allopatry), but when it did rarely occur, genetic exchange viral and bacterial lineages are some of the best-studied would only lead to hybrids that were unfit relative to their organisms in terms of their evolutionary origins and geno- progenitors. mic constitutions. The evolution of some of these disease- The review by Arnold and Hodges presented a challenge causing lineages has been traced across time, across differ- to the prevailing paradigm by providing examples of hybrid ent portions of the human and/or in different genotypes that did indeed run the gamut from less to more niches within the bodies of humans. These analyses have fit relative to their non-hybrid parents [1]. However, there not only provided tests for recombination between diver- were important deficiencies in the types of data considered gent lineages during the evolution of pathogens, but have in this review. First, Arnold and Hodges [1] only considered also highlighted the role such genetic exchange events eukaryotic groups, whereas it has been recognized for might have played in creating ‘hybrid’ organisms with decades that horizontal transfer between prokaryotic increased fitness. lineages can result in adaptive evolution (e.g. the acqui- sition of antibiotic resistance; [6]). Recently, this obser- Influenza By comparing yearly isolates of avian influenza viruses Corresponding author: Arnold, M.L. ([email protected]). from 1999 through 2004, Li et al. [9] were drawn to the

530 0169-5347/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2010.06.005 Trends in Ecology and Evolution 25 (2010) 530–536 Review Trends in Ecology and Evolution Vol.25 No.9 conclusion that the ‘H5N1’ viral lineage was endemic in exchange. Like influenza, this species evolves at an extre- Asian and that it presented a threat to mely high rate, with a significant proportion of its adaptive human populations through reassortment with human- change due to the exchange of genes between divergent associated H5N1 viruses. Indeed, such viral reassortants lineages. Also like the influenza studies discussed above, caused the influenza pandemics of 1918, 1957 and 1968; the analysis of samples collected across time and ecological pandemics that claimed hundreds of millions of lives [10]. setting provided the information necessary to identify Specifically, the 1918, 1957 and 1968 influenza strains better-adapted ‘hybrids.’ Ranging from the 1980’s to the originated from recombination events giving rise to gen- 2000’s, and from healthy adults to children suffering from a omes consisting of genes from viruses found in humans, of pathologies, the temporal and niche breadth other and birds [10]. The unique hybrid combi- encompassed in this study was extensive [12]. By sequen- nations of genes gave rise to viruses with increased patho- cing the genomes of these diverse isolates, it was concluded genicity that reflected an increased fitness relative to that horizontal transfers of various genes allowed the previous lineages. diversification of metabolic functions associated with niche Recently, the origin of a novel recombinant influenza adaptation in these E. coli strains [12]. lineage resulted in extensive, worldwide efforts by various Ogura et al. [13], studying a series of pathogenic, enter- governments and health agencies to reduce the possibility ohemorrhagic E. coli isolates, drew very similar con- of another pandemic. The so-called ‘swine-flu’ of 2009–2010 clusions to those of Touchon et al. [12] with regard to was, like all other influenza variants that infect humans, a the importance of gene acquisition to the adaptation of complex reassortant viral lineage (Figure 1) [11]. This bacterial species. Specifically, although the four enterohe- particular ‘H1N1’ virus is comprised of genes derived from morrhagic strains analyzed were not closely related phy- avian-, swine- and human-associated viral populations. By logenetically, they were found to share the same toxin examining samples across time and space, it was possible producing genes along with other genetic elements import- for Smith et al. [11] to identify the sources of all eight viral ant for their particular pathogenic niche [13]. The obser- genes (Figure 1) and to date the various divergence events vation that much of the remainder of the genomes of these of the genes. In particular, they concluded that: (i) PB2 and pathogens reflected divergent evolutionary histories, PA were of avian origin; (ii) PB1 came from a human virus; whereas the toxin genes indicated a recent common ances- (iii) HA, NP and NS were from one clade of swine influenza try, supported the hypothesis of the horizontal acquisition viruses; and (iv) NA and M originated from avian-like of the toxin loci. viruses found in Eurasian swine populations [11]. The mean divergence dates of these various components of Staphylococcus aureus the 2009 virus from other similar gene sequences were among bacterial species is well 1992 (N), 1997 (M) and 1998 (PB1, PB2, PA, H, NP, NS) established as a mechanism by which to new [11]. The divergence times were calculated using known niches are transferred or established [6]. As discussed dates of origin for some 20th Century viral lineages as above for E. coli, this is true for both commensal and parameters for a Bayesian analysis [11]. Thus, divergence pathogenic strains. Often, host shifts associated with and genetic exchange among viral lineages produced yet pathogens are thought of as being unidirectional; that is another fundamentally important human pathogen with from another animal lineage into human populations. apparently increased fitness (i.e. as estimated by its com- However, humans can act as the source host for pathogenic municability and virulence). strains found in other as well. The human-associated bacterial pathogen, Staphylococ- Escherichia coli cus aureus, is also a serious disease-causing agent in Touchon et al. [12] argued that the origin and adaptation of chickens, in which it causes skeletal infections. Genomic [(Figure_1)TD$IG]Escherichia coli strains were facilitated by genetic comparisons of S. aureus isolates collected from broiler chickens (over a 54-year-period), four other avian species, cows and , and humans allowed a test of the source and timing of transfer of this pathogen into broiler chicken populations [14]. The sampling scheme also provided a test of hypotheses concerning which genomic elements might have facilitated the host shift of S. aureus between animal lineages. The first conclusion reached from this analysis was that the pathogenic strain present in the worldwide popu- lation of broiler chickens originated from humans approxi- mately 38 ybp, with the variant in chickens being a member of a clonal subtype unique to human populations in Poland [14]. In addition, several genomic elements that might have contributed to the adaptive basis for this expansion of S. aureus into a novel niche were identified. Of particular interest to the topic of hybrid fitness, these genomic com- Figure 1. The species of origin for the genes contained in the ‘swine flu’ virus of ponents reflect horizontal exchange events that resulted in 2009. The genes originating from the avian, human and swine viral lineages are indicated next to the pictures of these organisms, and the red, blue and green bars the incorporation of numerous mobile genetic elements not indicate the constitution of the eight genes in this viral type [11]. found in human-associated S. aureus strains [14]. These

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and Widmer [19] proposed these as model systems for understanding the genetic and ecological underpinnings that influence hybrid fitness and .

Annual Sunflowers Rather than a simple bifurcating phylogeny, Rieseberg [20] proposed that the annual sunflowers were better-described as having a reticulate evolutionary history. Such a ‘web- like’ pattern of evolution is now known to be the rule, rather than the exception for many prokaryotic and eukar- yotic clades [7]. In the case of Helianthus, the weblike nature of evolution has given rise to numerous hybrid lineages. The evolutionary histories and ecological adap- tations of a number of these hybrid taxa have been defined (e.g. [21–25]). In the context of this review, one of the best-studied hybrid sunflower species is Helianthus paradoxus. The fitness of this species, relative to both parental and exper- Figure 2. The survivorship of Staphylococcus aureus strains from humans (MR1) imental hybrid genotypes, has been investigated across and chickens (ED98) exposed to either Avian or Human plasma [14]. time and habitats [24,26–28]. These studies have defined the genetic and phenotypic components that provide elev- elements included prophages, plasmids and pathogenicity ated fitness of H. paradoxus in extreme and novel environ- genes from a different staphylococcal lineage [14].The ments relative to its progenitor species, Helianthus annuus various mobile genetic elements incorporated into the broi- and Helianthus petiolaris. Rieseberg and his colleagues ler chicken genome were thus viewed as candidate, causal have thus inferred the following: (i) H. paradoxus’ occu- agents for the adaptations needed for the host shift from the pation of environments marked by elevated saline concen- human source population into chickens [14]. This host shift trations reflects an adaptation derived from its hybrid is characterized by a S. aureus strain that is more resistant genome; (ii) the adaptive possessed by this to the avian than is the strain from human hybrid species reflects transgressive trait expression (i.e. populations (Figure 2) [14]. In contrast, this strain is equally expression outside that of the parental phenotypic distri- fit relative to the human variant when exposed to com- butions); (iii) several QTL are associated with this pheno- ponents of the human immune system (Figure 2) [14].This type; and (iv) the expression of candidate loci that might new ‘hybrid’ bacterial lineage has thus apparently gained affect the saline-tolerance seen in H. paradoxus are adaptations to a novel niche (i.e. chickens) while at the same expressed differently in this species relative to its parental time retaining the adaptive machinery for the original, taxa [24,26–28]. Therefore, H. paradoxus reflects the elev- human host. ated fitness of some hybrid genotypes relative to parental lineages in certain (and in this case extreme) habitats. Fitness of hybrid plant genotypes Several plant groups have been analyzed across gener- Louisiana Irises ations in order to infer the fitness of hybrids relative to Beginning with work in the early part of the 20th Century, their parental lineages. For example, Campbell and her co- the Louisiana , consisting of Iris fulva, workers and Freeman and McArthur and their colleagues Iris hexagona, Iris brevicaulis and the hybrid species, Iris have performed long-term studies of parental and hybrid nelsonii, has been considered a paradigm for studies of lineages of Ipomopsis and Artemisia, respectively. Because hybridization and speciation [2,7,29]. For more than 20 of the extensive and long-term analyses carried out in both years, the goal of the research on this species assemblage of these genera, hybrid fitness across environments and life has been to understand the interaction between ecological history stages have been estimated (e.g. for Ipomopsis setting and genetic architecture on the transfer of genomic [15–17] and Artemisia [18]). However, for the purpose of material via introgressive hybridization and the establish- the present review, we will not discuss these examples in ment of hybrid lineages [7,29]. additional detail because, whereas there is excellent infor- With the above goal in mind, a series of genomic map- mation for both genera concerning the fitness of hybrid ping studies (involving multiple years and environments) classes (i.e. F1,F2 and backcrosses; [15,18]), detailed have been completed. These studies have allowed the fine- genetic data have yet to be reported. Long-term studies scale definition of genotype by environment interactions of two other plant species complexes are, however, avail- that affect variation in hybrid fitness. Genetic mapping able and these provide insights into the genotype by populations were created in 1999 between I. fulva and I. environment interactions affecting hybrid fitness. These brevicaulis by individuals between two clades are the annual sunflowers (Helianthus) and the these species into both of the parents [30]. After four years, Louisiana Irises (Iris). Lexer and Widmer [19] named these a QTL analysis was performed using survivorship as the as two of five complexes that have been developed into phenotype [31]. This analysis detected several QTL that model systems for understanding plant speciation. Of contributed to elevated hybrid fitness as reflected by an particular importance for the current discussion, Lexer increased likelihood of survivorship [31]. Five years after

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Figure 3. The observed frequencies of introgressed from either Iris fulva (filled circles) or Iris brevicaulis (open circles) into first generation backcross progeny formed from crosses between these two species. The X-axis indicates the genetic distances (in centimorgans) along each of the 21 linkage groups in the composite map. The Y-axis indicates the transmission ratio of either the I. fulva alleles or I. brevicaulis alleles introgressed into the backcrosses toward the alternate species. The expected frequency is 0.50 and is indicated by the dotted line. Data points above and below the solid lines indicate significant deviations from 0.50 (a = 0.05). Frequencies > 0.50 indicate an overrepresentation of either the I. fulva or I. brevicaulis alleles in the genetic background of the alternate species. Frequencies < 0.50 indicate an underrepresentation of these same categories [32]. the initial QTL analysis, another mapping experiment was rally with individuals from one or more other lineages carried out using the same populations to test for trans- [5,7,8,34]. For example, canids are well known for their mission ratio distortion (i.e. the degree to which loci tendency to participate in interspecific matings, with the deviated from the expected frequency of introgression; possible evolutionary and ecological outcomes of introgres- (Figure 3) [32]). This analysis detected genomic regions sion ranging from the threat of of rarer in which the frequency of introgression was higher, equiv- forms by more numerous congeners [35] to the facilitation alent to, or lower than the expected value (Figure 3). [(Figure_4)TD$IG] A recent study, in which the genotypes from the above mapping populations were placed into native habitats in southern Louisiana, USA, supported the conclusions drawn from the greenhouse experiments. Taylor et al. [33] recorded seven fitness components that encompassed both male and female contributions to sexual reproduction across two years and two environments. Their findings indicated that certain regions of the iris genome were prevented from recombining. In contrast, other regions reflected apparent adaptive introgression [33]. The results from this study, and those undertaken in the greenhouse environment, suggest the occurrence of hybrid genotypes that had higher, equivalent, or lower fitness than non- hybrid genotypes.

Fitness of hybrid animal genotypes Figure 4. The changeover in relative fitness of F1 hybrids between the Darwin’s in animal clades is not rare [7].In species, Geospiza fortis and Geospiza fuliginosa, before (low hybrid fitness) and after (high hybrid fitness) an El Nin˜ o event that profoundly altered the habitat some groups most members are known to hybridize natu- on the Gala´ pagos Island of Daphne Major [46].

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Figure 5. Introgressive hybridization linked with led to a significant decrease in the genetic and morphological (i.e. beak shape) divergence between the Darwin’s finch species, Geospiza scandens and Geospiza fortis over a >25-year period [49]. ‘Year 0’ indicates the first year data were collected. Though data were subsequently collected every year for 25 years, results are only presented at five-yearly time points. of adaptive evolution [36]. Likewise, it appears that at least analyses spanning more than three decades, they inferred a portion of the of the wonderfully the following: (i) environmental shifts due to climatic diverse African has resulted from genetic exchange perturbations (i.e. El Nin˜ oandLaNin˜ a events) resulted events between divergent lineages [37–41]. in an increase in the fitness of some hybrid genotypes (Figure 4) [46,47]; (ii) human-mediated habitat modifi- Darwin’s finches cations also increased hybrid fitness, thereby reducing Like plants, animal species complexes that demonstrate reproductive isolation between species [48]; (iii) both reticulate evolutionary histories have rarely been sub- genetic and phenotypic convergence were caused by a jected to both long-term ecological studies and detailed combination of interspecific gene flow and natural selec- genetic analyses. Thus, there are groups for which geno- tion (Figure 5) [49,50]; and (iv) hybrid genotypes acted as mic data have provided clear evidence for adaptive trait the source for new, reproductively isolated lineages introgression [42,43], yet which do not have across-year (Figure 6) [51]. Each of these inferences indicated that ecological data to test for genotype by environment inter- reticulate evolution within this group was pervasive and, actions. The single zoological example of an analysis that as indicated by Lowe [45], formed the basis for some of the combines both types of information is the archetype by adaptive evolution within this classic model system. In which all other such studies are judged, whether those the context of this review, the Geospiza findings reflect the study systems involve viruses, prokaryotes, plants or production of hybrid genotypes that demonstrate fitness animals. The example referred to is the work of Peter equivalent to, and in some cases greater than, their and Rosemary Grant and their colleagues on Darwin’s [(Figure_6)TD$IG]parental taxa. finches. The recognition that the genus Geospiza (i.e. Darwin’s finches) might have a reticulate, rather than a purely bifurcating, evolutionary history was foretold through observations made by Darwin and others. For example, in his book The Voyage of the Beagle [44], Darwin unintentionally described what one might expect from introgression when he stated, ‘The most curious fact is the perfect gradation in the size of the beaks in the different species of Geospiza, from one as large as that of a hawfinch to that of a chaffinch, and...even to that of a warbler...’ Some 80 years later Lowe [45] was explicit concerning the potential role of introgression in this group. He concluded that ‘...in the Finches of the Gala´- pagos we are faced with a swarm of hybridization seg- regates...’ Even though there were prior hints concerning the effect of hybridization within the Geospiza clade, it remained for the Grants and their colleagues to demon- Figure 6. The morphological divergence (as estimated from beak width) between a strate the important role of introgression, linked to resident population of Geospiza fortis (green bars) on the Gala´ pagos Island of Daphne Major and a lineage derived from the migration to the island of a G. fortis x natural selection, as an evolutionary catalyst. Specifi- G. scandens hybrid individual (yellow bars). The morphological distinctiveness of cally, using detailed ecological, life history and genetic these two classes of finch was reflective of premating reproductive isolation [51].

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Conclusions and future directions 6 Ochman, H. (2000) Lateral gene transfer and the nature of bacterial The combination of ecological analyses carried out across innovation. Nature 405, 299–304 7 Arnold, M.L. (2006) Evolution through Genetic Exchange, Oxford Univ. years or generations, with the collection of detailed genetic Press data sets, has provided a much greater definition of the 8 Grant, P.R. and Grant, B.R. (1992) Hybridization of bird species. environmental correlates, the genetic architecture and the Science 256, 193–197 adaptive aspects of hybrid fitness. The major take home 9 Li, K.S. et al. (2004) Genesis of a highly pathogenic and potentially message from the above discussion is that when genomes pandemic H5N1 influenza virus in eastern Asia. Nature 430, 209–213 10 Smith, G.J.D. et al. (2009) Dating the of pandemic influenza recombine there is a release of genetic and phenotypic viruses. Proc. Natl. Acad. Sci. U.S.A. 106, 11709–11712 variability that makes adaptive change possible [2–7]. 11 Smith, G.J.D. et al. (2009) Origins and evolutionary genomics of the Whether viruses, bacteria, plants or animals are con- 2009 swine-origin H1N1 influenza A epidemic. Nature 459, 1122–1126 sidered, the potential is the same for generating novel 12 Touchon, M. et al. (2009) Organised genome dynamics in the genetic architectures that can be less, equivalent or more Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5 (1), e1000344 (doi:10.1371/journal.pgen.1000344) fit in parental or novel habitats. This was the inference of 13 Ogura, Y. et al. (2009) Comparative genomics reveal the mechanism of Arnold and Hodges in 1995 [1]. Yet, the rigorous testing of the of O157 and non-O157 enterohemorrhagic their inference has only been possible through the types of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 106, 17939–17944 studies discussed above. 14 Lowder, B.V. et al. (2009) Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc. The biological examples in this review come from a Natl. Acad. Sci. U.S.A. 106, 19545–19550 diverse array of the domains of life. However, they reflect 15 Campbell, D.R. et al. (2008) Lifetime fitness in two generations of the few available studies that combine long-term ecological Ipomopsis hybrids. Evolution 62, 2616–2627 analyses with the genomic information necessary to infer 16 Campbell, D.R. and Waser, N.M. (2007) Evolutionary dynamics of an estimates of hybrid fitness and the evolutionary role of Ipomopsis : confronting models with lifetime fitness data. Am. Nat. 169, 298–310 adaptive, genetic exchange. In other words, there exists a 17 Wu, C.A. and Campbell, D.R. (2006) Environmental stressors very limited set of analyses that address the topic of differentially affect leaf ecophysiological responses in two Ipomopsis reticulate evolutionary processes using such an exper- species and their hybrids. Oecologia 148, 202–212 imental design. The component that is normally (but not 18 Miglia, K.J. et al. (2005) Nine-year reciprocal transplant experiment in always, see [15–18]) missing are data from ecological stu- the gardens of the basin and mountain big sagebrush (Artemisia tridentata: Asteraceae) hybrid zone of Salt Creek Canyon: the dies across habitats and generations. The explanation for importance of multiple-year tracking of fitness. Biol. J. Lin. Soc. 86, the missing data sets most likely reflects the difficulties in 213–225 finding funding for such analyses as well as with the 19 Lexer, C. and Widmer, A. (2008) The genic view of plant speciation: logistics of keeping the fieldwork proceeding over many recent progress and emerging questions. Phil. Trans. R. Soc. B 363, years. Because of the dearth of such combined analyses, we 3023–3036 20 Rieseberg, L.H. (1991) Homoploid reticulate evolution in Helianthus are left with the question of how often hybrid genotypes (Asteraceae): evidence from ribosomal genes. Am. J. Bot. 78, 1218– exceed their parents in fitness and thus reflect adaptive 1237 trait introgression or adaptive hybrid speciation. Yet, the 21 Whitney, K.D. et al. (2010) Adaptive introgression of abiotic tolerance above studies provide the evidence of how powerful such traits in the sunflower Helianthus annuus. New Phytol. 187, 230–239 22 Whitney, K.D. et al. (2006) Adaptive introgression of herbivore long-term experimental programs can be in identifying resistance traits in the weedy sunflower Helianthus annuus. Am. unexpected patterns of ecological and evolutionary change Nat. 167, 794–807 [47]. These types of studies will continue to be one of the 23 Gross, B.L. et al. (2004) Reconstructing the origin of Helianthus most rigorous approaches for testing hypotheses concern- deserticola: survival and selection on the desert floor. Am. Nat. 164, ing not only hybrid fitness, but also the role of genetic 145–156 24 Rieseberg, L.H. et al. (2003) Major ecological transitions in wild exchange in adaptive evolution. sunflowers facilitated by hybridization. Science 301, 1211–1216 25 Welch, M.E. and Rieseberg, L.H. (2002) Patterns of Disclosure Statement suggest a single, ancient origin for the diploid hybrid species The authors declare that there are no conflicts of interest Helianthus paradoxus. Evolution 56, 2126–2137 that would inappropriately influence this work. 26 Donovan, L.A. et al. (2009) Phenotypic selection on leaf ecophysiological traits in Helianthus. New Phytol. 183, 868–879 27 Edelist, C. et al. 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