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Simultaneous Quaternary Radiations of Three Damselfly Clades Across

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Simultaneous Quaternary Radiations of Three Damselfly Clades Across vol. 165, no. 4 the american naturalist april 2005 E-Article Simultaneous Quaternary Radiations of Three Damselfly Clades across the Holarctic Julie Turgeon,1,2,* Robby Stoks,1,3,† Ryan A. Thum,1,4,‡ Jonathan M. Brown,5,§ and Mark A. McPeek1,k 1. Department of Biological Sciences, Dartmouth College, the evolution of mate choice in generating reproductive isolation as Hanover, New Hampshire 03755; species recolonized the landscape following deglaciation. These anal- 2. De´partement de Biologie, Universite´ Laval, Que´bec, Que´bec yses suggest that recent climate fluctuations resulted in radiations G1K 7P4, Canada; driven by similar combinations of speciation processes acting in dif- 3. Laboratory of Aquatic Ecology, University of Leuven, Chemin ferent lineages. de Be´riotstraat 32, B-3000 Leuven, Belgium; 4. Department of Ecology and Systematics, Cornell University, Keywords: Enallagma, speciation, radiation, amplified fragment Ithaca, New York 14850; length polymorphism (AFLP), mtDNA, phylogeny. 5. Department of Biology, Grinnell College, Grinnell, Iowa 50112 Submitted October 22, 2004; Accepted December 27, 2004; The fossil record recounts recurrent cycles of mass ex- Electronically published February 9, 2005 tinction immediately followed by rebounds in biodiversity throughout Earth’s history (Jablonski 1986, 1994; Benton 1987; Raup 1991; Sepkoski 1991). A few of these events profoundly reshaped global biodiversity (e.g., the end- abstract: If climate change during the Quaternary shaped the Permian mass extinction erased up to 96% of the world’s macroevolutionary dynamics of a taxon, we expect to see three fea- species; Raup 1979; Jablonski 1994; but see Raup 1991), tures in its history: elevated speciation or extinction rates should date but most of these have been more limited in their taxo- to this time, more northerly distributed clades should show greater nomic scope (Raup 1991). Climatic upheavals over the discontinuities in these rates, and similar signatures of those effects past 1.65 million years have had similar, though less severe, should be evident in the phylogenetic and phylodemographic his- effects on the world’s biota. Repeated glacial advances and tories of multiple clades. In accordance with the role of glacial cycles, speciation rates increased in the Holarctic Enallagma damselflies dur- retreats during the Pleistocene caused shifting and frag- ing the Quaternary, with a 4.25# greater increase in a more northerly mentation of species ranges across the globe to the extent distributed clade as compared with a more southern clade. Finer- that many fossil assemblages 10,000–20,000 years ago have scale phylogenetic analyses of three radiating clades within the north- little resemblance to extant assemblages, even though ern clade show similar, complex recent histories over the past 250,000 many of the same species still exist (Overpeck et al. 1992; years to produce 17 Nearctic and four Palearctic extant species. All Holman 1993; Coope 1995; Graham et al. 1996; see also three are marked by nearly synchronous deep splits that date to reviews by Hewitt 1996, 2004). These events drove extinct approximately 250,000 years ago, resulting in speciation in two. This was soon followed by significant demographic expansions in at least many species that presumably could not respond rapidly two of the three clades. In two, these expansions seem to have pre- enough to both the direct consequences of changes in the ceded the radiations that have given rise to most of the current physical environment and indirect consequences resulting biodiversity. Each also produced species at the periphery of the clade’s from interacting with different species (Kurte´n and An- range. In spite of clear genetic support for reproductive isolation derson 1980; Martin and Klein 1984). Along with extinc- among almost all species, mtDNA signals of past asymmetric hy- tions, climatic fluctuations also produced range fragmen- bridization between species in different clades also suggest a role for tations, shifts, bottlenecks, and subsequent expansions, the consequences of which presumably generated ideal geo- * E-mail: [email protected]. graphic, demographic, ecological, genetic, and social con- † E-mail: [email protected]. ditions to promote speciation in taxa as well (e.g., Carson ‡ E-mail: [email protected]. and Templeton 1984; Vrba 1985; Coyne and Orr 2004). § E-mail: [email protected]. However, the importance of recent climatic oscillations k Corresponding author; e-mail: [email protected]. to the macroevolutionary dynamics of various taxa re- Am. Nat. 2005. Vol. 165, pp. E78–E107. ᭧ 2005 by The University of Chi- mains controversial. For example, the mammal fossil rec- cago. 0003-0147/2005/16504-40696$15.00. All rights reserved. ord shows substantial faunal turnover and recent and rapid Worldwide Radiation of Damselflies E79 speciation in many taxa (Kurte´n and Anderson 1980; Lister rates, whereas taxa at lower latitudes should show less 2004), but analyses of molecular distances between sister change. Moreover, taxa whose macroevolutionary dynam- taxa in birds have failed to support a recent upturn in ics were shaped by the same climate event should all show avian speciation rates (Klicka and Zink 1997, 1999; Zink coincident signatures of those dynamics in multiple clades, et al. 2004). Likewise, fossil and subfossil collections of if more than one clade survived (e.g., altered diversification beetles show little change over the Quaternary and are rates, range fragmentation, bottlenecks, and expansions; largely composed of still extant species (Coope 2004), but Rogers and Harpending 1992; Rogers 1995). Speciation phylogenetic analyses of the Cicindela tiger beetles do show and extinction rates can be evaluated directly for taxa with a weak trend for elevated speciation rates during the last a good Quaternary fossil record (e.g., beetles: Coope 1995, million years (Barraclough and Vogler 2002; see also 2004; mammals: Kurte´n and Anderson 1980; Lister 2004), Knowles 2000, 2001; Knowles and Otte 2000 for another but for most taxa that do not have adequate fossil records, insect example). No general statement can be made about indirect methods must be utilized (e.g., Nee et al. 1992, the predominant responses of plants to climatic changes 1994). during the Quaternary either; the dominant response of In this article, we examine the diversification history of arborescent species was extinction rather than speciation the Enallagma damselflies (Zygoptera: Coenagrionidae) or stasis, but speciation rates of vascular plants often in- across the Holarctic to test whether Quaternary climate creased during periods of glaciation (Willis and Niklas change shaped the macroevolutionary dynamics of this 2004). clade. First, we test the degree to which species that have Clearly, not all taxa have responded similarly to recent been shown in previous studies to share mtDNA haplo- climatic oscillations. Many different factors may influence types are reproductively isolated from one another by an- whether and how taxa are affected by such climatic events. alyzing a large amplified fragment length polymorphism First and foremost, biogeography would seem to be crucial; (AFLP) data set. Next, we add sequences from four Pa- taxa inhabiting higher latitudes should be more affected learctic Enallagma species and one more Nearctic species by glacial events than taxa at lower latitudes. Phylogeo- to the data set of Brown et al. (2000) and reanalyze this graphic studies suggest this to be the case, with northerly larger data set to test whether speciation and extinction distributed species showing strong phylogeographic signals rates in the genus have changed recently and whether the of recent range fragmentation and expansions, whereas magnitudes of discontinuities differ between more north- more southerly distributed species show phylogenetic sig- erly and more southerly distributed clades. Finally, we an- nals characteristic of stable long-term occupancy of their alyze a much larger mtDNA data set to reconstruct the ranges (Bernatchez and Wilson 1998; Hewitt 2004; Martin phylogenetic and phylodemographic histories of the three and McKay 2004). Vagility should also strongly influence radiating clades. If these three clades radiated in response the tempo of range shifts and the degree of isolation that to recent climatic events, we expect similar phylogenetic may be generated from range fragmentations (Coope 1995, and phylodemographic patterns across the three clades. 2004). Vagile taxa may respond to climate change by rap- idly shifting their ranges, while less vagile taxa may be more susceptible to extinction and may be most likely to The Study System diversify following climatic upheavals (Dynesius and Jans- son 2000; Jansson and Dynesius 2002; but see Bouchard The Enallagma damselflies provide an amazing example and Brooks 2004). Species inhabiting relatively uncommon of a taxon that appears to have very recently radiated to or ephemeral environmental conditions may also be more produce continent-wide faunas. With 38 described species, likely to be driven extinct than species inhabiting relatively Enallagma is one of the two most speciose odonate genera common environment types. Similarly, species with broad in North America (the anisopteran genus Gomphus also ecological tolerances are expected to be less affected than has 38 North American species; Westfall and May 1996). taxa with more narrow ecological needs (e.g., Knowles Previous phylogenetic
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