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Incomplete Lineage Sorting and Hybridization in the Evolutionary

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Incomplete Lineage Sorting and Hybridization in the Evolutionary RESEARCH ARTICLE AMERICAN JOURNAL OF BOTANY Incomplete lineage sorting and hybridization in the evolutionary history of closely related, endemic yellow-fl owered Aechmea species of subgenus Ortgiesia (Bromeliaceae)1 Márcia Goetze 2 , Camila M. Zanella 2,3 , Clarisse Palma-Silva 4 , Miriam V. Büttow2,5 , and Fernanda Bered 2,6 PREMISE OF THE STUDY: The yellow-fl owered Aechmea subgenus Ortgiesia (yfAsO) (Bromeliaceae) is a group of seven morphologically similar bromeliads found mostly in the southern Brazilian Atlantic rainforest. The recent origin of this group probably contributes to its taxonomic complexity. The aims of this study were to investigate the levels of genetic diversity and structure at the population and species levels, to gain insight into the processes behind the diversifi cation of the group, and to contribute to the establishment of species boundaries. METHODS: We sequenced two noncoding regions of the chloroplast genome ( rpl32-trnL and rps16-trnK ) and the nuclear phyC gene in 204 and 153 indi- viduals, respectively, representing the seven species of the group. Phylogeographical and population genetics approaches were used. KEY RESULTS: Three of the seven yfAsO showed some degree of genetic diff erentiation among species. Divergence time for the group was dated to around 4 million years ago. Areas of conservation value were identifi ed, and a scenario of multiple refugia in the southern Brazilian Atlantic rainforest during the Pleistocene climatic oscillations is suggested. CONCLUSIONS: We hypothesized that incomplete lineage sorting and localized hybridization events are responsible for the low levels of genetic diff eren- tiation and the taxonomic complexity observed among and within the seven yfAsO species. Further studies on Aechmea comata and Aechmea kertesziae will be necessary to clarify the boundary between these two species. Most of the populations sampled showed high genetic diversity and/or unique haplotypes; they should be prioritized for conservation purposes. KEY WORDS Brazilian Atlantic rainforest; Bromeliaceae; diversifi cation; evolutionary history; genetic diversity; genetic structure; multiple refugia; phylogeography; Pleistocene Speciation has fascinated evolutionary biologists since Darwin’s 2010 ). Geographical isolation and adaptation to new ecological time. Despite much research into the ecological and genetic mecha- conditions are among the main factors invoked to explain the ap- nisms involved in speciation, many questions remain ( Sobel et al., pearance of new species ( Lorenz-Lemke et al., 2010; Pavan et al., 2011 ; Hope et al., 2012 ; Fregonezi et al., 2012 ; Gehring et al., 2013 ; 1 Manuscript received 10 March 2017; revision accepted 15 May 2017. Wachowiak et al., 2013 ; Turchetto et al., 2014 ; Gao et al., 2015 ). 2 Universidade Federal do Rio Grande do Sul, Instituto de Biociências, Programa de Pós- Th ese factors may lead to novel genetic combinations, thus giving graduação em Genética e Biologia Molecular, Avenida Bento Gonçalves 9500, P.O. Box rise to divergent populations and distinct genetic lineages ( Seehausen, 15053 91501-970, Porto Alegre, RS, Brazil; 2004 ). Studies focusing on the distribution of genetic diversity are 3 Th e John Bingham Laboratory, National Institute of Agricultural Botany (NIAB), Huntingdon Road, CB30LE, Cambridge, UK; of great importance to understand intra- and interspecifi c genetic 4 Universidade Estadual Paulista Júlio de Mesquita Filho, Instituto de Biociências, Programa diff erentiation. In particular, the investigation of closely related de Pós-graduação em Ecologia e Biodiversidade, Avenida 24A 1515 13506-900, Rio Claro, congeners can shed light on their evolutionary relationships and SP, Brazil; and the processes involved in their diversifi cation (Hewitt, 2001 ; López- 5 Fundação Estadual de Pesquisa Agropecuária—Fepagro Serra do Nordeste, Distrito de Fazenda Souza 95125-000, Caxias do Sul, RS, Brazil Vinyallonga et al., 2015 ; Slovák et al., 2015 ; Feng et al., 2016 ). 6 Author for correspondence (e-mail: [email protected]) Recently diversified related species frequently show complex https://doi.org/10.3732/ajb.1700103 genetic patterns. In plants, these can mostly be explained by AMERICAN JOURNAL OF BOTANY 104 (7): 1073 – 1087 , 2017; http://www.amjbot.org/ © 2017 Botanical Society of America • 1073 1074 • AMERICAN JOURNAL OF BOTANY incomplete lineage sorting and hybridization/introgression pro- incomplete lineage sorting and possible hybridization events cesses ( Rieseberg, 1997 ; Bouillé and Bousquet, 2005 ; Abbott et al., ( Goetze et al., 2016b ). All these features contribute to the taxo- 2013 ; Gaudeul et al., 2014 ; Segatto et al., 2014 ; Slovák et al., 2015 ). nomic issues within this subgenus. During speciation, both processes may result in shared genetic vari- Here, we combined data from chloroplast (cp) DNA and nuclear ation and, as a consequence, in nonmonophyletic species ( de genomes and applied phylogeographical and population genetics Queiroz, 2007). To pinpoint which of them is responsible for the approaches to obtain insight into the processes driving the diversi- complex genetic scenario seen is a challenging task ( Joly et al., 2009 ; fi cation and to contribute to the establishment of species boundar- Seehausen et al., 2014 ), but the geographical pattern of genetic vari- ies in the yfAsO. We investigated patterns of genetic structure and ation across species can provide useful insights. While incomplete diversity within the yfAsO at both population and species levels, lineage sorting leads to a spread-out pattern of shared genetic varia- across most of the group’s geographical range. Our specifi c aims tion, hybridization/introgression is normally coincident with sym- were (1) to examine whether morphologically identifi ed species are patric occurrence of species ( Palme et al., 2004; Mims et al., 2010; genetically diff erentiated and to thus clarify species boundaries; (2) Gaudeul et al., 2014 ; Segatto et al., 2014 ; Gao et al., 2015). Both in- to identify hybridization events among yfAsO species and to shed complete lineage sorting and hybridization/introgression are oft en light on their role in the diversifi cation process and species delimi- observed in taxa that are products of recent adaptive radiation, a tation; and (3) to quantify genetic diversity and its distribution process in which an evolutionary group experiences diversifi cation among populations, with the goal of identifying areas of conserva- into a variety of ecological niches in an extremely short amount of tion value. time ( Gavrilets and Losos, 2009 ). Th erefore, these taxa may have had no time to accumulate specifi c polymorphisms or alleles that could diff erentiate between them. Likewise, reproductive barriers MATERIALS AND METHODS preventing gene fl ow between diverging populations may be in- complete ( Nosil et al., 2009 ; Mims et al., 2010 ). Species description— Th e geographical range of the seven yfAsO Th e genus Aechmea (Bromeliaceae) includes ~280 species with a species (Appendix S1, see Supplemental Data with the online ver- geographical distribution ranging from Mexico to Uruguay ( Smith sion of this article) extends from the Brazilian state of São Paulo to and Downs, 1979 ; Luther, 2012 ). It has undergone a rapid diversifi - Rio Grande do Sul (latitudes of 23 ° to 29° S), with the range of a cation process, especially within the Brazilian Atlantic rainforest single species extending into Argentina ( Smith and Downs, 1979 ; ( Schulte et al., 2005 , 2009 ; Silvestro et al., 2014 ; Goetze et al., 2016b ). Reitz, 1983 ; Goetze et al., 2016b ; Fig. 1 ). Within this group, Aech- Phylogenetic studies have demonstrated that the genus is polyphy- mea caudata Lindm. is the most widespread species. It can be epi- letic, presenting a serious taxonomic challenge ( Faria et al., 2004 ; phytic, terrestrial, or saxicolous and occurs in both mountainous Horres et al., 2007 ; Schulte et al., 2005 , 2009 ; Schulte and Zizka, 2008 ; and coastal areas. Aechmea blumenavii Reitz is restricted to the Sass and Specht, 2010; Silvestro et al., 2014; Heller et al., 2015 ). As northern area of the Brazilian state of Santa Catarina, occurring in part of the core bromelioids clade, which originated around 5 mil- the forest at elevations above 500 m a.s.l., mostly as an epiphyte, lion years ago (Ma), Aechmea is also an example of a group that has while Aechmea kertesziae Reitz grows on rocks or as a terrestrial diversifi ed relatively recently (Schulte et al., 2009; Givnish et al., and is found only in the coastal region of Santa Catarina state. 2011 ; Silvestro et al., 2014 ). Aechmea comata Baker and Aechmea kleinii Reitz are narrowly re- Th e subgenus Ortgiesia is one of the eight subgenera described stricted species, the former occurring only in the coastal regions of within the genus Aechmea ( Smith and Downs, 1979 ). In a previous Santa Catarina Island, the latter on the continent at elevations study based on AFLP markers, we showed that these taxa are above 1000 m a.s.l., both in Santa Catarina state. Aechmea comata genetically close related, although their evolutionary relationships can be epiphytic, terrestrial or saxicolous, while A. kleinii grows remain unresolved ( Goetze et al., 2016b ). Based on morphology, mostly as an epiphyte. Aechmea winkleri Reitz is a disjunct species two main groups of species are observed within Aechmea subgenus limited to two regions, which are around 480 km from one another Ortgiesia : one has yellow
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