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Adaptive Radiations: from Field to Genomic Studies

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Adaptive Radiations: from Field to Genomic Studies Adaptive radiations: From field to genomic studies Scott A. Hodges and Nathan J. Derieg1 Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106 Adaptive radiations were central to Darwin’s formation of his phenotype–environment correlation, (iii) trait utility, and (iv) theory of natural selection, and today they are still the centerpiece rapid speciation. Monophyly and rapid speciation for many of for many studies of adaptation and speciation. Here, we review the the classic examples of adaptive radiation have been established advantages of adaptive radiations, especially recent ones, for by using molecular techniques [e.g., cichlids (4), Galapagos detecting evolutionary trends and the genetic dissection of adap- finches (5, 6), and Hawaiian silverswords (7)]. Ecological and tive traits. We focus on Aquilegia as a primary example of these manipulative experiments are used to identify and test pheno- advantages and highlight progress in understanding the genetic type–environmental correlations and trait utility. Ultimately, basis of flower color. Phylogenetic analysis of Aquilegia indicates such studies have pointed to the link between divergent natural that flower color transitions proceed by changes in the types of selection and reproductive isolation and, thus, speciation (3). anthocyanin pigments produced or their complete loss. Biochem- Studies of adaptive radiations have exploded during the last 20 ical, crossing, and gene expression studies have provided a wealth years. In a search of the ISI Web of Science with ‘‘adaptive of information about the genetic basis of these transitions in radiation’’ (limited to the subject area of evolutionary biology) Aquilegia. To obtain both enzymatic and regulatory candidate we found 80 articles published in 2008 compared with only 1 in genes for the entire flavonoid pathway, which produces antho- 1990. Furthermore, citations of these articles have grown expo- cyanins, we used a combination of sequence searches of the nentially, from 34 citations in 1990 to Ͼ3,000 in 2008. The Aquilegia Gene Index, phylogenetic analyses, and the isolation of growing interest in adaptive radiations may be ascribed to several novel sequences by using degenerate PCR and RACE. In total we factors. First, molecular phylogenetics has allowed the identifi- identified 34 genes that are likely involved in the flavonoid cation of monophyly and rapid speciation in taxa outside of the pathway. A number of these genes appear to be single copy in traditionally-recognized examples from isolated islands and Aquilegia and thus variation in their expression may have been key lakes (e.g., ref. 8) and thus has expanded the repertoire of study for floral color evolution. Future studies will be able to use these systems. Second, there has been a resurgence in the study of sequences along with next-generation sequencing technologies to speciation (9). Speciation research has often focused on the follow expression and sequence variation at the population level. development of genetic incompatibilities (e.g., refs. 10 and 11), The genetic dissection of other adaptive traits in Aquilegia should whereas studies of adaptive radiations have focused attention on also be possible soon as genomic resources such as whole-genome the role of divergent natural selection to alternate environments sequencing become available. as a primary cause of reproductive isolation (3, 12–15). Thus, studies of adaptive radiations focus on both the evolution of anthocyanins ͉ evolutionary trend ͉ flower color ͉ hybrid zone adaptations and reproductive isolation. Understanding the processes of adaptation and speciation re- daptive radiations have played, and continue to play, a quires considering taxa that have not yet fully attained reproductive Acentral role in the development of evolutionary theory. isolation. Fundamentally, the ability to make hybrids allows the After his exploration of the Galapagos Islands, Darwin recog- dissection of the genetic basis of traits and permits tests of how nized that variants of species were confined to specific islands. individual genetic elements could affect individual fitness. For In particular, Darwin (1) noted that mockingbirds he collected example, Bradshaw and Schemske (16) made near-isogenic lines of on different islands represented 3 distinct forms and that all of Mimulus cardinalis and Mimulus lewisii, each containing the alter- the forms were similar to mockingbirds from the mainland of nate allele from the other species for a flower color locus. They South America. He further noted that the different islands were found that pollinator visitation patterns radically changed and that, within sight of one another, all quite similar in their habitats, and in the proper ecological setting, an adaptive shift in pollinator apparently geologically young. Based on these observations, preference could possibly occur with a single mutation (16). In Darwin (2) began to suspect that species gradually became addition, studying speciation and adaptation early in the process has modified. Thus, began his search for a process that could account significant advantages because subsequent genetic changes can for such observations, leading to his formulation of the theory of obscure the actual causal mutations (ref. 17; see also ref. 82). For natural selection. example, loss-of-function mutations that confer an adaptive advan- Key to Darwin’s suspicion of common ancestry was the close tage may be followed by additional mutations that would, on their proximity of environmentally-similar islands comprising the own, cause loss of function but were not involved with the evolution Galapagos archipelago. In fact, many classic examples of adap- of the trait itself (18). Thus, recent adaptive radiations are especially tive radiations involve islands or lakes; notable examples include fruitful resources for dissecting the genetic basis of adaptations and Darwin’s finches of the Galapagos, honeycreeper birds and speciation. silversword plants of Hawaii, and cichlid fish of lakes Malawi and Adaptive radiations have also played a major role in identi- Victoria in Africa. The power of these examples for inferring the fying evolutionary trends. This area of study is important be- force of natural selection in evolution stems from the marked diversity in form and function among a group of clearly closely- related taxa. The isolation of islands and lakes makes plausible This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, ‘‘In the Light of Evolution III: Two Centuries of Darwin,’’ held January 16–17, 2009, the inference that the taxa are descended from a single ancestor, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and and the link between variation in form and function makes Engineering in Irvine, CA. The complete program and audio files of most presentations are credible the notion that natural selection and evolution have available on the NAS web site at www.nasonline.org/Sackler࿝Darwin. played key roles. Author contributions: S.A.H. and N.J.D. designed research, performed research, analyzed A great deal of research effort has gone into substantiating the data, and wrote the paper. assumptions behind examples of adaptive radiation. In an influ- The authors declare no conflict of interest. ential book, Schluter (3) laid out the definition of adaptive This article is a PNAS Direct Submission. radiation as having 4 features: (i) common ancestry, (ii)a 1To whom correspondence should be addressed. E-mail: [email protected]. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0901594106 PNAS ͉ June 16, 2009 ͉ vol. 106 ͉ suppl. 1 ͉ 9947–9954 Downloaded by guest on September 29, 2021 cause trends imply predictable patterns in evolutionary history. pollinators will avoid visiting flowers whose nectar reward they There has been, for example, much debate about whether body cannot reach. Recently these alternative hypotheses were explic- size and complexity increase through time (19–23). One way to itly tested with a species-level phylogeny of the North American test for repeatable trends has been to test whether the evolution adaptive radiation of Aquilegia (38). Transitions between major of particular traits is associated with species diversity. For classes of pollinators were found to be significantly directional, example, clades of flowering plants that have independently consisting of bee to hummingbird and hummingbird to hawk- evolved floral nectar spurs show a statistically significant trend moth but no reversals and no bee to hawkmoth transitions. for increased species diversity compared with nonspurred clades Concomitant with these shifts were increases in spur length. In (24–26). This finding has led to the nectar spurs being consid- addition, models of the tempo of evolution strongly indicated the ered a ‘‘key innovation’’ with the implication that they mecha- concentration of spur-length evolution at times of speciation. nistically increase the likelihood of speciation. Thus, as with the broad correlation between the evolution of Another way to test for trends during evolutionary history is spurs themselves and species diversity, this study suggests that to test explicitly for directionality of trait evolution on a phy- spur length is intimately linked with the speciation process, at logeny. Critical to such analyses is the reconstruction of ancestral least in North American species of Aquilegia (38, 39). Function- states (27, 28).
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