Modern Quaternary Plant Lineages Promote Diversity Through Facilitation of Ancient Tertiary Lineages
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Modern Quaternary plant lineages promote diversity through facilitation of ancient Tertiary lineages Alfonso Valiente-Banuet*†, Adolfo Vital Rumebe*, Miguel Verdu´ ‡, and Ragan M. Callaway§ *Departamento de Ecologı´ade la Biodiversidad, Instituto de Ecologı´a,Universidad Nacional Auto´noma de Me´xico, A.P. 70-275, C.P. 04510 Me´xico D.F., Me´xico; ‡Centro de Investigaciones sobre Desertificación, Consejo Superior de Investigaciones Científicas, Universitat de València, Generalitat Valenciana, Cami de la Marjal s͞n Apartado Oficial, Albal, 46470 Valencia, Spain; and §Division of Biological Sciences, University of Montana, Missoula, MT 59812 Edited by Gordon H. Orians, University of Washington, Seattle, WA, and approved September 25, 2006 (received for review June 14, 2006) One of the most important floristic sorting periods to affect analyzed the relationship between the evolutionary histories (the modern plant communities occurred during the shift from the wet periods when particular taxa evolved) of taxa in Mediterranean- Tertiary period to the unusually dry Quaternary, when most global climate plant communities and how these same taxa interact with deserts developed. During this time, a wave of new plant species other species during recruitment. Specifically, we compared the emerged, presumably in response to the new climate. Interest- importance of facilitative interactions for recruitment between ingly, most Tertiary species that have been tracked through the contemporary Tertiary and Quaternary taxa in Mediterranean- fossil record did not disappear but remained relatively abundant type communities around the world by integrating biogeo- despite the development of a much more unfavorable climate for graphic, paleobotanical, and ecological literature. We asked species adapted to moist conditions. Here we find, by integrating whether recent species, those that evolved during the xeric paleobotanical, ecological, and phylogenetic analyses, that a large Quaternary and presumed to possess drought-tolerant traits, number of ancient Tertiary species in Mediterranean-climate eco- facilitate ancient species that evolved during the mesic Tertiary systems appear to have been preserved by the facilitative or and are presumed to be less drought-tolerant. ‘‘nurse’’ effects of modern Quaternary species. Our results indicate The ecology and evolution of Mediterranean-type ecosystems that these interdependent relationships among plants have played are well studied (2, 3, 9–13), and although these climatic regions a central role in the preservation of the global biodiversity and occupy Ͻ5% of the Earth’s surface, they harbor almost 20% of provided a mechanism for stabilizing selection and the conserva- the known vascular plant species diversity on Earth. As in other tion of ecological traits over evolutionary time scales. ecosystems, Mediterranean-climate communities are the result of historical effects and sorting processes occurring in different ͉ ͉ Mediterranean-type ecosystems Mexical shrubland phylogenetic niche geological times and different ecological scenarios (3, 13). ͉ ͉ conservatism plant facilitation stabilizing selection Many extant taxa in Mediterranean climates originated in the Tertiary [65 to 2 million years (Myr) B.P.] (9, 10) and now are he evolutionary processes that drive speciation and create mixed with recent taxa that evolved at the end of Tertiary and Tbiological diversity are central to the natural sciences, but we beginning of the Quaternary (2 Myr B.P., post-Pliocene) during know little regarding the historical ecological processes that have a period when global climate became much more arid, a change eliminated species from communities or allowed them to persist that has lasted until today (13). In fact, the current Mediterra- (1). Current plant communities are the product of historical nean climate emerged during the Quaternary (8), corresponding sorting processes and, therefore, include mixtures of floristic with the extinction of a substantial component of Tertiary taxa. elements originating in different geological times and, presum- Based on paleobotanical evidence (9, 10), the archetypal ever- ably, under different ecological scenarios (2). Many extant plant green sclerophyllous vegetation of modern Mediterranean-type species are millions of years old (3) and, therefore, have persisted vegetation is relictual of the Madrean-Tethyan vegetation of the through dramatic changes in global climate. Biogeographic and Tertiary, which originally existed in a belt around North America paleontological evidence indicates that communities are derived and Eurasia where the climate was warm and wet climate. from species that have originated in different geological times Relictual Madrean-Tethyan taxa, or the Laurisilva, can be and places, and that these taxa have been mixed and culled observed today in the isolated northern Atlantic Canary archip- independently of each other through various sorting processes ielago (9, 14). During most of the Tertiary, sclerophyllous shrubs (2, 3). The perception that interdependent processes among constituted the understory of a rich oak-laurel-madrone wood- plant species are insignificant over evolutionary time frames has lands, and these shrubs expanded geographically in response to been central to the idea that communities are ‘‘merely a coin- the drying climate during the Eocene (55 Myr B.P.) and the cidence’’ (4) and the development of neutral model theory on Oligocene (36 Myr B.P.) (9, 10). Despite the wave of extinctions biodiversity (5). Therefore, with few exceptions (6, 7), plant that occurred with increasing aridity, the fossil record shows that communities are not thought to possess stable properties deter- large taxonomic components of this ancient flora remain in mined by plant–plant interactions. contemporary communities of Mediterranean regions (3, 9, 10) In contrast to existing theory, our observations of ecological and tropical non-Mediterranean regions (13, 15) around the relationships among species in semiarid communities around the world and include some of the most abundant modern genera world suggest that powerful facilitative ecological interactions among plant species have been a crucial component of the historical and sorting processes responsible for the composition Author contributions: A.V.-B. and A.V.R. designed research; A.V.-B., A.V.R., M.V., and and diversity of contemporary plant communities. Facilitative R.M.C. performed research; A.V.-B., A.V.R., M.V., and R.M.C. contributed new reagents͞ interactions appear to have been particularly important during analytic tools; A.V.-B., A.V.R., M.V., and R.M.C. analyzed data; and A.V.-B., A.V.R., M.V., and the shift from mesic Tertiary period to the unusually dry R.M.C. wrote the paper. Quaternary when global deserts developed. Desertification pro- The authors declare no conflict of interest. vided a strong stimulus for the emergence of new taxa (8), but This article is a PNAS direct submission. many Tertiary species, adapted to moist conditions, did not go Abbreviations: Myr, million years; OU, Ornstein–Uhlenbeck. extinct despite the development of a progressively drier climate †To whom correspondence should be addressed. E-mail: [email protected]. but remained relatively abundant (3, 9). We quantitatively © 2006 by The National Academy of Sciences of the USA 16812–16817 ͉ PNAS ͉ November 7, 2006 ͉ vol. 103 ͉ no. 45 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0604933103 Downloaded by guest on September 24, 2021 such as Rhus, Cercocarpus, Garrya, Ceanothus, Arctostaphylos, recruitment of species that evolved in the Tertiary period than Pistacia, Quercus, and Dodonaea. for the recruitment of species that evolved in the Quaternary As groups, Tertiary and Quaternary taxa differ substantially period. Of the 113 taxa across all six examined regions that were in life-history and reproductive traits (3, 13). Indeed, analysis of identified as evolving during the Tertiary from the fossil record, life history-reproductive traits across woody genera in Mediter- 86 were identified in the literature (or measured by us) as ranean ecosystems indicates two sharply contrasting life-history recruiting significantly more beneath the canopies of other syndromes that are consistently associated with evolutionary species than in the open (Table 1 and Fig. 1, for all regions origin (3, 13). The most important traits distinguishing Tertiary combined X 2 ϭ 103.3; P Ͻ 0.0001). In contrast, taxa that were and Quaternary syndromes are fruit type (fleshy vs. nonfleshy identified from the fossil record as evolving in the Quaternary fruits) and seed size, which are directly related to the regener- recruited preferentially in open spaces and avoided the canopies ation niche (3). Many fleshy-fruited Tertiary species have been of other species; 97 of 100 Quaternary species recruited in the reported to depend of the facilitative effects of other species to open rather than under nurse plants. This pattern was most establish (12, 16). In contrast, dry-fruited Quaternary species pronounced in California (X 2 ϭ 27.06; P Ͻ 0.0001), the Medi- often are reported to recruit in open microsites without other terranean basin (X 2 ϭ 40.44; P Ͻ 0.0001), Chile (X 2 ϭ 8.12; P ϭ species, such as caused by recurrent Mediterranean fires (12). 0.018), and the Mexical (X 2 ϭ 18.17; P Ͻ 0.0001). South Africa Based on this potential relationship between ancestry and (X 2 ϭ 4.54; P ϭ 0.067) and Australia (data did not allow to run regeneration life history traits, we predicted