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Phylogeography Above the Species Level for Perennial Species in a Composite Genus

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Phylogeography Above the Species Level for Perennial Species in a Composite Genus Research Article Phylogeography above the species level for perennial species in a composite genus Karin Tremetsberger1,2*, Marı´aA´ ngeles Ortiz1, Anass Terrab1, Francisco Balao1, Ramo´n Casimiro-Soriguer1,3, Marı´a Talavera1 and Salvador Talavera1 1 Departamento de Biologı´a Vegetal y Ecologı´a, Universidad de Sevilla, Apdo. 1095, 41080 Seville, Spain 2 Present address: Institute of Botany, Department of Integrative Biology and Biodiversity Research, University of Natural Resources and Life Sciences, Gregor Mendel Straße 33, 1180 Vienna, Austria 3 Present address: Departamento de Biologı´a, CASEM, Universidad de Ca´diz, Campus Rı´o San Pedro, 11510 Puerto Real, Spain Received: 22 April 2015; Accepted: 11 November 2015; Published: 7 December 2015 Associate Editor: Chelsea D. Specht Citation: Tremetsberger K, Ortiz MA´ , Terrab A, Balao F, Casimiro-Soriguer R, Talavera M, Talavera S. 2016. Phylogeography above the species level for perennial species in a composite genus. AoB PLANTS 8: plv142; doi:10.1093/aobpla/plv142 Abstract. In phylogeography, DNA sequence and fingerprint data at the population level are used to infer evolution- ary histories of species. Phylogeography above the species level is concerned with the genealogical aspects of divergent lineages. Here, we present a phylogeographic study to examine the evolutionary history of a western Mediterranean composite, focusing on the perennial species of Helminthotheca (Asteraceae, Cichorieae). We used molecular markers (amplified fragment length polymorphism (AFLP), internal transcribed spacer and plastid DNA sequences) to infer rela- tionships among populations throughout the distributional range of the group. Interpretation is aided by biogeographic and molecular clock analyses. Four coherent entities are revealed by Bayesian mixture clustering of AFLP data, which correspond to taxa previously recognized at the rank of subspecies. The origin of the group was in western North Africa, from where it expanded across the Strait of Gibraltar to the Iberian Peninsula and across the Strait of Sicily to Sicily. Pleis- tocene lineage divergence is inferred within western North Africa as well as within the western Iberian region. The exist- ence of the four entities as discrete evolutionary lineages suggests that they should be elevated to the rank of species, yielding H. aculeata, H. comosa, H. maroccana and H. spinosa, whereby the latter two necessitate new combinations. Keywords: Amplified fragment length polymorphism; Helminthotheca; Iberian Peninsula; phylogeography; Strait of Gibraltar; western Mediterranean region; western North Africa. Introduction mitochondrial, plastid and nuclear genomes. The field of Intraspecific phylogeography as originally defined by phylogeography today extends from the level of conspe- Avise et al. (1987) is concerned with the geographic distri- cific populations to the supraspecific level (Avise 2000) bution of genealogical lineages at the level of conspecific and targets organisms from the bacteria and eukaryote populations. Originally based upon animal mitochondrial domains of life as well as viruses. Phylogeography of closely DNA sequence data, phylogeographic studies today related species spans the boundary between reticulate and make use of a variety of molecular techniques and are divergent relationships, where a partially braided collection based upon DNA sequence and fingerprint data from the of allelic pathways of interbreeding individuals bifurcates * Corresponding author’s e-mail address: [email protected] Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properlycited. AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015 1 Tremetsberger et al. — Phylogeography in the western Mediterranean into two such collections (Avise 2000). Likewise, genea- The most recent common ancestor (MRCA) of extant logical data at the population level of closely related spe- taxa of Helminthotheca can be traced back to the Plio- cies are especially helpful for explaining distributions cene or Pleistocene (Tremetsberger et al. 2013). It is resulting from historical and ecological factors. thus likely that populations have been affected by cli- A region that offered many opportunities for ecogeo- matic changes occurring in the Mediterranean region in graphic and effective geographic isolation (Sobel et al. this epoch, possibly leading to range shifts, disruptions 2010) due to its variegated geologic and climatic history of previously continuous ranges and secondary contacts. since the Miocene is the western Mediterranean region. This study aims at shedding light on the evolutionary his- The formation of the Betic-Rif orogen led to the desicca- tory of the perennial species of Helminthotheca.Using tion of the Mediterranean Sea between 6 and 5.3 million molecular makers from the nuclear and plastid genomes, years ago (mya; Hsu¨ et al. 1973), enabling the migration we addressed the following questions: (i) Does genetic of animals and plants between the two continents grouping correlate with the present taxonomic treat- (Bocquet et al. 1978). At the end of the Messinian, the ment? (ii) Where did perennial species of Helminthotheca Strait of Gibraltar opened and water from the Atlantic originate? (iii) Along which routes did they spread to Ocean refilled the dry Mediterranean Basin (Lonergan occupy their present areas? The inferred evolutionary his- and White 1997), thus again disconnecting north-western tory is discussed with respect to the evolutionary forces Africa from south-western Europe. that might have been relevant for speciation. Major climatic events after the opening of the Strait of Gibraltar were the advent of the Mediterranean climate Methods and Pleistocene climatic oscillations. In northern Africa, the appearance of a local or temporary dry season was Plant material already recognizable in the floristic composition of the We sampled populations belonging to subspecies of Hel- Miocene and this climate trend was accentuated in the minthotheca aculeata and H. comosa in Algeria, Italy Pliocene (Que´zel 1978). In the north-western Mediterra- (Sicily), Morocco, Portugal and Spain (Table 1,Fig.1). nean area, a Mediterranean climatic rhythm with sum- Helminthotheca echioides was included as outgroup. Vou- mer drought appeared in the Pliocene, at 3.2 mya chers of all populations used are deposited in the herbaria (Suc 1984). In the Pleistocene, the water level of the Medi- at Seville (SEV) and/or Vienna (WU). The Algerian species terranean Sea underwent great oscillations. During the H. balansae and H. glomerata (Que´zel and Santa 1963) last glacial maximum (0.02 mya), it was 120 m lower could not be sampled for this study. In the field, leaves than today, so that the oceanic barrier between north- from individual plants were conserved in silica gel. Distri- western Africa and south-western Europe was much bution ranges of the taxa under study were compiled reduced in extension, though not completely disrupted from survey of material in the herbaria at Barcelona (Thiede 1978). The western Mediterranean region was (BC),Geneva(G),Madrid(MA),Montpellier(MPU),Paris an important refugium for temperate as well as Mediter- (P), Salamanca (SALA) and Seville (SEV). Locations men- ranean plants and animals during the Pleistocene glacial tioned in Pignatti (1982) and Sauvage (1961) were also periods (Me´dail and Diadema 2009). It is supposed that used. DIVA-GIS ver. 7.1.7.2 (Hijmans et al. 2001)was the changing environmental conditions and appear- used to display distribution ranges and sample locations. ance/disappearance of biogeographic barriers have mas- sively triggered plant and animal diversification in the Amplified fragment length polymorphism (AFLP) Pliocene and Pleistocene (Fiz-Palacios and Valca´rcel The protocol for extraction of genomic DNA from silica 2013). gel-dried leaves, restriction-ligation (EcoRI and MseI), The genus Helminthotheca (Asteraceae, Cichorieae, Hypo- preselective and selective amplification, and electro- chaeridinae) has a primarily western Mediterranean distribu- phoresis on a capillary sequencer (3130xl Genetic Ana- tion. It has been separated from Picris at the generic level on lyzer, Applied Biosystems) exactly followed Tremetsberger the basis of the conspicuously enlarged outer involucral et al. (2009). Three selective primer combinations bracts and comprises the annual, heterocarpic species [EcoRI(Fam)-ACA/MseI-CAT,EcoRI(Vic)-AGG/MseI-CTCand H. echioides and H. balansae and the perennial, homocarpic EcoRI(Ned)-AAC/MseI-CTT] were selected following a pri- species H. aculeata, H. comosa and H. glomerata (Picris mer trial testing 12 selective primer combinations, based comosa auct. alg.; Lack 1974, 1975). Helminthotheca acu- on the criteria of interpretability (presence/absence), leata has another subspecies, H. aculeata subsp. maroccana, spread of bands in the region 50–500 bp, and number of in addition to the nominal subspecies. Similarly, H. comosa bands (70–90 per primer combination). Raw data were also has another subspecies, H. comosa subsp. lusitanica, aligned with the GeneScan 500 ROX size standard using in addition to the nominal subspecies. ABI PRISM GeneScan ver. 3.71 (&Applied Biosystems). 2 AoB PLANTS www.aobplants.oxfordjournals.org
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