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Comparative Phylogeography COLLOQUIUM INTRODUCTION John C COLLOQUIUM INTRODUCTION In the light of evolution X: Comparative phylogeography COLLOQUIUM INTRODUCTION John C. Avisea,1, Brian W. Bowenb, and Francisco J. Ayalaa Phylogeography is the study of the spatial arrange- evolutionary histories is ensconced in nuclear genomes ment of genealogical lineages, especially within and that are increasingly accessible to scrutiny. Section III among conspecific populations and closely related focuses on comparative phylogeography in a taxonomic species (10). Ever since its inception in the late 1970s sense, emphasizing how phylogeographic findings (11, 12) and mid-1980s (13), the field has sought to have impacted ecological and evolutionary thought in extend phylogenetic reasoning to the intraspecific level, a diversity of organismal groups. Section IV focuses on and thereby build empirical and conceptual bridges be- comparative phylogeography in a conceptual sense by tween the formerly separate disciplines of microevolu- addressing the place of phylogeography in relation to tionary population genetics and macroevolutionary various allied disciplines in the biodiversity sciences. phylogenetics. In the early years, phylogeographers Several papers in these proceedings inevitably over- relied on data from restriction-site surveys of mito- lap in their sectional assignments because (for exam- chondrial (mt) DNA to draw inferences about population ple) disparate taxa tend to inhabit different environments, structure and historical demography, but stunning im- and because the researchers assembled here had a provements in molecular techniques (14, 15) and exten- diversity of phylogeographic objectives, data types, sions of coalescent theory and other analytical methods and analytical approaches. (16) later broadened the field’s scope dramatically (17). Phylogeographic perspectives have transformed aspects Comparative Phylogeography in a Spatial Sense of population biology, biogeography, systematics, ecol- Phylogeographers have roamed the planet in their ogy, genetics, and biodiversity conservation. One aim of quest to identify patterns that might typify organisms this colloquium was to bring together leading scientists occupying diverse environmental regimes. Understand- to address the current state of phylogeography as the ing the biotic response to past challenges provides a discipline enters its fourth decade. The broader goal compass for contemporary and future challenges. was to update a wide audience on recent developments Brian Bowen et al. (19) summarize a vast literature on in phylogeographic research and their relevance to past phylogeographic findings for the world’s oceans. At accomplishments and future research directions. face value, the oceanic realm might seem to be fea- Many of the advancements in phylogeography tureless and relatively free of impediments to gene have entailed comparative appraisals of one sort or flow. Nevertheless, many migrant species in the sea another (18). (See refs. 1–9 for papers from previous (such as marine turtles, and some cetaceans and pelagic colloquia in the series and Box 1 for an overview of the fishes) display phylogeographic patterns, implicating series.) Papers in Section I of this colloquium empha- physical barriers as promoters of both intraspecific size the word “comparative” in a spatial sense, where genetic breaks and subsequent allopatric speciation the phylogeographic assessments entail various spe- events (properly viewed as stages along a temporal cies (sometimes generally codistributed) that may be continuum). For marine taxa more generally, a wide representative of particular kinds of environmental variety of phylogeographic outcomes implies the op- settings, such as oceanic versus continental realms. eration of other evolutionary processes as well, such as Section II deals with comparative phylogeography in sympatric or ecological speciation in some cases, en- a genomic sense. Nonrecombining cytoplasmic ge- vironmental effects from historically shifting climates, nomes have been the standard workhorses of genea- and the important role of organismal behavior and logical analyses, but in principle the primary library of natural history in shaping current phylogeographic aDepartment of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697-2525; and bHawai’i Institute of Marine Biology, Kane’ohe, HI 96744 This paper serves as an introduction to the PNAS Colloquium articles, which resulted from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “In the Light of Evolution X: Comparative Phylogeography,” held January 8–9, 2016, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. It is the 10th (and final) in a series of colloquia under the umbrella title “In the Light of Evolution” (see Box 1). The complete program and video recordings of most presentations are available ontheNASwebsiteatwww.nasonline.org/ILE_X_Comparative_Phylogeography. Papers from previous colloquia in the series appear in refs. 1–9. Author contributions: J.C.A., B.W.B., and F.J.A. wrote the paper. The authors declare no conflict of interest. 1To whom correspondence should be addressed. Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1604338113 PNAS Early Edition | 1of5 Downloaded by guest on September 28, 2021 and much research in the previous century, is transforming into a more nuanced and multifactorial perspective on why Box 1. In the Light of Evolution. In 1973, Theodosius Dobz- lineages are distributed as we observe them today. hansky penned a short commentary titled “Nothing in biology Ivan Prates et al. (21) use a case-history approach to reveal how makes sense except in the light of evolution” (35). Most sci- historic climate and habitat changes affected three broadly entists agree that evolution provides the unifying framework codistributed lizard species in Amazonia and the Atlantic Forest of for interpreting biological phenomena that otherwise can the Neotropics. This study finds partial congruence in phylogeo- often seem unrelated and perhaps unintelligible. Given the graphic patterns that can be attributable to shared historical in- central position of evolutionary thought in biology, it is sadly fluences plus similarities in life history and environmental needs. ironic that evolutionary perspectives outside the sciences have However, the authors then go much further by embracing the been neglected, misunderstood, or purposefully misapplied. close link between phylogeographic pattern and historic population Biodiversity—the great variety of life—is an exuberant product demography to deduce that these taxa had species-specific pop- of the evolutionary past, a vast support system for the con- ulation demographies in their recent past. These demographic pa- temporary human endeavor (aesthetic, intellectual, and ma- rameters (in conjunction with ecological niche models related to terial), and a rich legacy to cherish and preserve for the future. climate change) forecast very distinct population trajectories over the Two challenges, as well as opportunities, for 21st century next 60 y for these three environmentally sensitive lizard species. science are to gain deeper insights into the evolutionary Remote oceanic archipelagos offer especially intriguing evo- processes that foster biodiversity and to translate that un- lutionary studios for studying phylogeographic processes on iso- derstanding into workable solutions for the regional and lated chains of islands that originated (typically in sequential global crises wrought by seven billion people. A grasp of temporal order) via hotspot volcanism. These midoceanic islands evolutionary principles and processes is important in other offer a proverbial tabula rasa in which every species has origins societal arenas as well, such as education, medicine, sociol- elsewhere, and community composition is stilted by the filter of ogy, and applied fields, including agriculture, pharmacology, dispersal ability. Several such oceanic archipelagos are scattered and biotechnology. The ramifications of evolutionary thought around the world’s oceans, in most cases with the islands being extend into learned realms that are traditionally the domain displaced unidirectionally by plate tectonic movements, as if on of philosophy and religion. The central goal of the “In the Light an evolutionary conveyor belt. Kerry Shaw and Rosemary Gillespie of Evolution” series has been to promote the evolutionary (22) review comparative phylogeographic findings for diverse taxa sciences through state-of-the-art colloquia and published on six such oceanic archipelagos. They focus especially on the proceedings. Each installment has explored evolutionary “progression rule,” which predicts that older genealogical line- perspectives on a particular biological topic that is scientifi- ages should map to older islands within an archipelago, with cally intriguing but also has special relevance to contemporary progressively younger lineages mapping to progressively youn- societal issues or challenges. Individually and collectively, the ger islands within each such island chain. Shaw and Gillespie find “In the Light of Evolution” series has aimed to interpret phe- support for the progression rule in some cases (notably in the nomena in various areas of biology through the lens of evo- Hawaiian archipelago), but less so on some others. The authors lution, address some of the most intellectually vital as well also highlight the precedence effect,
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