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1127 Lichens Are Mutualistic Associations Between a Fungus (Mycobiont) and Photosynthetic Green Algae And/Or Cyano- Bacteria, Th

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1127 Lichens Are Mutualistic Associations Between a Fungus (Mycobiont) and Photosynthetic Green Algae And/Or Cyano- Bacteria, Th American Journal of Botany 101 ( 7 ): 1127 – 1140 , 2014 . E COLOGICAL SPECIALIZATION IN T REBOUXIA (TREBOUXIOPHYCEAE) PHOTOBIONTS OF R AMALINA MENZIESII ( RAMALINACEAE) ACROSS SIX RANGE-COVERING ECOREGIONS 1 OF WESTERN NORTH AMERICA S ILKE W ERTH 2–4,6 AND V ICTORIA L. SORK 2,5 2 Department of Ecology and Evolutionary Biology, University of California Los Angeles, Box 957239, Los Angeles, California 90095-7239 USA; 3 Faculty of Life and Environmental Sciences, University of Iceland, Sturlugata 7, 101 Reykjavík, Iceland; 4 Biodiversity and Conservation Biology, Swiss Federal Research Institute WSL, Zürcherstrasse 111, CH-8903 Birmensdorf, Switzerland; and 5 Institute of the Environment and Sustainability, University of California Los Angeles, Box 951496, Los Angeles, California 90095-1496 USA • Premise of the study: Many lichens exhibit extensive ranges spanning several ecoregions. It has been hypothesized that this wide ecological amplitude is facilitated by fungal association with locally adapted photobiont strains. • Methods: We studied the identity and geographic distribution of photobionts of the widely distributed North American lichen Ramalina menziesii based on rbcL (chloroplast DNA) and nuclear ribosomal ITS DNA sequences. To test for ecological spe- cialization, we associate photobiont genotypes with local climate and phorophyte. • Key results: Of the photobiont lineages of R. menziesii , 94% belong to a clade including Trebouxia decolorans. The remaining are related to T. jamesii . The photobionts showed (1) signifi cant structure according to ecoregion and phorophyte species and (2) genetic associations with phorophyte species and climate. • Conclusions: Geography, climate, and ecological specialization shape genetic differentiation of lichen photobionts. One great advantage of independent dispersal of the fungus is symbiotic association with locally adapted photobiont strains. Key words: ecological specialization; genetic differentiation; host plant specifi city; lichenized ascomycetes; phorophyte; photobiont ; Ramalina menziesii ; Ramalinaceae; symbiosis; Trebouxia decolorans ; Trebouxiophyceae. Lichens are mutualistic associations between a fungus cyanobacterial species participating in the lichen symbiosis (mycobiont) and photosynthetic green algae and/or cyano- are often able to persist outside of the lichen thallus ( Bubrick bacteria, the so-called photobionts ( Richardson, 1999 ). The et al., 1984 ; Mukhtar et al., 1994 ; Wirtz et al., 2003 ; O’Brien symbiosis is obligate for the fungus, but the green algal and et al., 2005 ; Sanders, 2005 ). Given that lichens require a mu- tualistic associate to exist, one might think that this require- ment for two compatible taxa to fi nd each other would 1 Manuscript received 18 January 2014; revision accepted 11 June 2014. The authors thank D. Kofranek, A. R. Plüss, G. Segelbacher, D. Stone, constrain their distribution geographically and to specifi c and C. T. Winder for fi eld assistance and K. Lundy and E. Martinez for environmental conditions. Instead, many species are wide- technical assistance. K. Dillman, K. Gaddis, N. Hillyard, K. Knudsen, B. spread on different continents, albeit in the same habitat type McCune, P. Rundel, and P. Thompson kindly provided additional samples ( Otte et al., 2002 , 2005 ). For instance, the lichen Cetraria of R. menziesii . Funding for this research was provided by a National aculeata (Schreb.) Fr. occurs in temperate, arctic, and ant- Geographic Award to V.L.S. and S.W., postdoctoral fellowships from arctic environments ( Fernández-Mendoza et al., 2011 ), while the Swiss National Foundation (PBBEA-111207) and the European Cavernularia hultenii Degel. occurs disjunctly on two conti- Commission within FP7 (LICHENOMICS) to S.W., a UCLA Senate nents in similar forest types ( Printzen et al., 2003 ). Then research award, UCLA Life Science funds, and a National Science again, other species range continuously across multiple cli- Foundation award (DEB-0089445) to V.L.S. They acknowledge the matic zones and ecosystems. For instance, Niebla cephalota University of California Natural Reserve System, where they performed fi eldwork at Sedgwick Reserve and Santa Cruz Island Reserve administered (Tuck.) Rundel & Bowler ranges from the desert of southern by UC Santa Barbara, Hastings Natural History Reservation and Angelo Baja California to the coniferous forest in the State of Wash- Coast Range Reserve (UC Berkeley), McLaughlin Natural Reserve and ington ( Brodo et al., 2001 ), and Ramalina menziesii Taylor Quail Ridge Reserve (UC Davis), and Landels-Hill Big Creek Reserve is distributed from coastal deserts of Baja California to tem- (UC Santa Cruz). The following agencies granted collecting permits: perate rain forests of Alaska ( Sork and Werth, 2014 ). California State Parks, Oregon State Parks, Washington State Parks, The high dispersal potential of lichens is amplifi ed by their Channel Islands Natl. Park, Point Reyes Natl. Seashore, Olympic Natl. ability to tolerate environmental stress. Because lichens are poi- Park, Pacifi c Rim Natl. Park, Pender Islands Natl. Park, Gwaii Hanas Natl. kilohydric organisms, their metabolism approaches zero when Park, Baja California Sur & Norte protected and natural areas. For logistical they dry out, allowing them to tolerate extreme conditions support, they thank P. Aigner, V. Boucher, J. Delgadillo, B. Huebel, C. Koehler, O. Lee, L. Laughrin, K. McCurdy, K. Merg, R. Skillin, P. Steel, ( Nash, 2008 ). For example, two lichen species survived expo- M. Stromberg, S. Swarbrick, and M. Williams. sure to space conditions on an earth-orbiting satellite, and back 6 Author for correspondence (e-mail: [email protected] , [email protected] ) on Earth they approached normal photosynthetic rates within 1 d after hydration ( Sancho et al., 2007 ). The presence of doi:10.3732/ajb.1400025 lichens in extreme environments in the Arctic and Antarctic, American Journal of Botany 101 ( 7 ): 1127 – 1140 , 2014 ; http://www.amjbot.org/ © 2014 Botanical Society of America 1127 1128 AMERICAN JOURNAL OF BOTANY [Vol. 101 and in desert regions ( Rundel, 1978 ; Castello and Nimis, ( Werth and Sork, 2008 ). Given that the photobionts were 1997 ; Domaschke et al., 2012 ; Pérez-Ortega et al., 2012 ) pro- within dispersal range of each other, this fi nding raises the vides additional evidence of their unusual level of tolerance. possibility that the genetic differentiation was due to local se- Yet, this greatly enhanced ability to tolerate environmental lection pressures on the algal genotypes. stress and extreme conditions is not present separately in each Previously we studied the phylogeography of the widespread partner of the mutualism ( de Vera et al., 2008 ). Thus, the mutu- lichen fungus R. menziesii in coastal areas of western North alists seem to synergistically create a symbiotic phenotype that America using DNA sequences of four nuclear low-copy genes has environmental tolerances greater than the fungal species and found genetic differentiation among ecoregions, but no sig- and photobiont separately. nifi cant divergence associated with the phorophyte species One mechanism for creating such an adaptable phenotype is ( Sork and Werth, 2014 ). Here we address two central hypothe- association with specifi c photobiont strains. Many lichen fungi ses concerning the photobiont of the lichen R. menziesii : (1) disperse through microscopic ascospores and then “relichen- that Trebouxia photobionts should show strong genetic differ- ize” with a local photobiont partner, which is likely to be entiation across major ecoregions due to (a) restricted gene fl ow adapted to those local ecological conditions ( Piercey-Normore over topographic and climate barriers between ecoregions and and DePriest, 2001 ; Yahr et al., 2006 ; Werth, 2011 ). For ex- (b) selection by local environmental conditions that amplifi es ample, ecologically similar but taxonomically unrelated lichen genetic differences and (2) that Trebouxia photobionts are eco- fungi often share closely related photobiont strains ( Lücking logically specialized on different phorophyte species within et al., 2009 ; Peksa and Škaloud, 2011 ). The photobionts associat- ecoregions, leading to genetic differentiation of photobionts ing with individual lichen fungi exhibit large-scale geographic sampled from different phorophyte species. Specifi cally, we trends related to ecology and biogeography ( Yahr et al., 2006 ; have three goals. Our fi rst aim is to identify the lineages of Wornik and Grube, 2010 ; Fernández-Mendoza et al., 2011 ; Trebouxia associating with R. menziesii throughout its range Widmer et al., 2012 ). While some mycobionts are highly selec- using a phylogenetic approach. Second, we quantify the hierar- tive for photobiont strains ( Yahr et al., 2004 ; Fedrowitz et al., chical genetic structure associated with ecoregion and phoro- 2011 , 2012 ; Dal Grande et al., 2012 ; Werth and Scheidegger, phyte species within ecoregion to fi nd evidence for the second 2012 ), other lichen fungi associate with a wide range of taxa hypothesis. Third, we conduct separate multivariate ordination ( Blaha et al., 2006 ; Nyati et al., 2013 ) or with divergent photobi- analyses to test for associations with local phorophyte species ont species or strains in different parts of their ranges ( Altermann, and climate environments. Our fi ndings will highlight patterns 2009 ; Nelsen and Gargas, 2009 ). Fungal selectivity for photo- of genetic diversity and differentiation of an understudied, yet bionts
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