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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/331592845 Being in the right place at the right time? Parallel diversification bursts favored by the persistence of ancient epizoochorous traits and hidden factors in Cynoglossoideae Article in American Journal of Botany · March 2019 DOI: 10.1002/ajb2.1251 CITATIONS READS 5 566 4 authors: Ana Otero Pedro Jiménez-Mejías Spanish National Research Council Universidad Autónoma de Madrid 13 PUBLICATIONS 38 CITATIONS 142 PUBLICATIONS 1,496 CITATIONS SEE PROFILE SEE PROFILE Virginia Valcárcel Pablo Vargas Universidad Autónoma de Madrid Spanish National Research Council 62 PUBLICATIONS 711 CITATIONS 539 PUBLICATIONS 7,084 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Evolutionary history of Antirrhinum genus View project Completion of the Euro+Med Plantbase View project All content following this page was uploaded by Pedro Jiménez-Mejías on 13 March 2019. The user has requested enhancement of the downloaded file. RESEARCH ARTICLE Being in the right place at the right time? Parallel diversification bursts favored by the persistence of ancient epizoochorous traits and hidden factors in Cynoglossoideae Ana Otero1,2,4,5 , Pedro Jiménez-Mejías3,4, Virginia Valcárcel3,4, and Pablo Vargas1 Manuscript received 8 October 2018; revision accepted 14 January PREMISE OF THE STUDY: Long- distance dispersal (LDD) syndromes, especially endozoochory, 2019. facilitate plant colonization of new territories that trigger diversification. However, few 1 Departamento de Biodiversidad, Real Jardín Botánico, CSIC. Pza. de studies have analyzed how epizoochorous fruits influence both range distribution and Murillo, 2, 28014 Madrid, Spain diversification rates. We examined the evolutionary history of a hyperdiverse clade of 2 Escuela Internacional de Doctorado, Universidad Rey Juan Boraginaceae (subfamily Cynoglossoideae, eight tribes, ~60 genera, ~1100 species) and Carlos, C/Tulipán s/n, 28933 Móstoles, Spain the evolution of fruit traits. We evaluated the evolutionary history of diaspore syndromes 3 Centro de Investigación en Biodiversidad y Cambio Global (CIBC- UAM), Universidad Autónoma de Madrid, 28049 Madrid, Spain correlated with geographic distribution and diversification rates over time. 4 Departamento de Biología (Botánica), Facultad de Ciencias METHODS: Plastid DNA regions and morphological traits associated with dispersal Biológicas, Universidad Autónoma de Madrid, C/ Darwin, 2, 28049 syndromes were analyzed for 71 genera (226 species). We employed trait- dependent Madrid, Spain diversification analysis (HiSSE) and biogeographic reconstruction (Lagrange) using a 5 Authors for correspondence (e-mail: [email protected], [email protected]) time- calibrated phylogeny. Citation: Otero, A., P. Jiménez-Mejías, V. Valcárcel, and P. Vargas. KEY RESULTS: Our results indicate that (1) the earliest divergence events in Cynoglossoideae 2019. Being in the right place at the right time? Parallel diversification occurred in the central- northeastern Palearctic during the Paleogene (early to middle bursts favored by the persistence of ancient epizoochorous traits Eocene); (2) an epizoochorous trait (specialized hooks named glochids) is ancestral and has and hidden factors in Cynoglossoideae. American Journal of Botany 106(3): 1–15. been maintained long term; and (3) glochids are correlated with increased diversification doi:10.1002/ajb2.1251 rates in two distantly related clades (Rochelieae and Cynoglossinae). Rapid speciation occurred for these two groups in the same area (central- eastern Palearctic) and same period (Oligocene- Miocene: Rochelieae, 30.82–13.69 mya; Cynoglossinae, 33.10–15.21 mya). Lower diversification rates were inferred for the remaining four glochid- bearing clades. CONCLUSIONS: One more example of “biogeographic congruence” in angiosperms is supported by a shared geographic (central- northeastern Palearctic) and temporal (28.60–21.59 mya, late Oligocene) opportunity window for two main clades’ diversification. Epizoochorous traits (fruit glochids) had an effect in higher diversification rates only with the joint effect of other unmeasured factors. KEY WORDS biogeography; Boraginaceae; diversification rates; HiSSE; hyperdiverse; phylogeny; trait-dependent reconstruction; historical contingency. Fleshy fruit innovations appearing in late Cretaceous angiosperms increases the chances of establishing new populations and con- have long been associated with the diversification of vertebrates sequently promoting speciation (see Beaulieu and Donoghue, that acted as seed dispersers (Regal, 1977). Indeed, mammal and 2013). Likewise, the acquisition of a trait related to biotic disper- bird diversification during the Cenozoic would have favored the sal is a key innovation that may have boosted diversification rates evolution of fruits specialized for both internal (endozoochory) in many taxonomic groups (e.g., endozoochory in Myrtaceae and external (epizoochory) dispersal by vertebrates (Burger, [Biffin et al., 2010] and endozoochory and epizoochory in Fagales 1981; Tiffney, 1986, 2004). Biotic dispersal also favors geographic [Larson- Johnson, 2016]). However, while the acquisition or loss range expansion through the colonization of new areas, which of a single trait may promote diversification, the cumulative action American Journal of Botany 106(3): 1–15, 2019; http://www.wileyonlinelibrary.com/journal/AJB © 2019 Botanical Society of America • 1 2 • American Journal of Botany of various factors must be invoked in the spatiotemporal context 2014). Interestingly, even though Cynoglossoideae is the most of each particular lineage (e.g., see “synnovation” in Donoghue diversified subfamily, a notable unevenness of species diversity and Sanderson, 2015). exists among the lineages. There are many rare, endemic genera Long- distance dispersal (LDD) has many biogeographic im- (e.g., Gyrocaryum, Myosotidium, Suchtelenia, Antiotrema) that plications; it explains the movement of diaspores over dispersal contrast with highly diversified and widely distributed lineages barriers to distant territories, between continent and islands, (e.g., Lappula, Cynoglossum, Myosotis, Mertensia) (Chacón et al., and within large continents. Previous studies indicated that LDD 2016). through epizoochory is relatively rare (<5% of all angiosperm Integrative analyses of historical biogeography and diversi- species studied in 10 regional floras [Sorensen, 1986]; 5.2% for the fication rates are needed to properly evaluate whether diaspore entire flora of Europe [Heleno and Vargas, 2015]), and that epizo- specializations related to LDD have been driving factors in mac- ochorous traits are less effective than endozoochorous traits, es- roevolutionary patterns of speciation, extinction, and dispersal pecially with avian vectors (Costa et al., 2014; Heleno and Vargas, (Beaulieu and Donoghue, 2013; Larson- Johnson, 2016). The high 2015). Despite low occurrence in angiosperms, epizoochorous number of widespread clades and lineages of Cynoglossoideae that traits have been invoked to explain species connections via in- occur in more than three continents (five lineages:Trichodesma , tercontinental (Vargas et al., 1999) and continent-island dispersal Myosotis, Lappula, Mertensia, and Hackelia; two clades: subtribe (Heleno and Vargas, 2015). Indeed, Sorensen (1986) proposed Cynoglossinae and tribe Omphalodeae) and the predominance of that epizoochory is able to successfully disperse diaspores over fruit specializations related to LDD syndromes (Otero et al., 2014) larger geographic scales than all other LDD syndromes (i.e., fruit offer a unique opportunity to assess the role of diaspore traits in specializations related to LDD: anemochory, thalassochory, en- historical biogeography and diversification. dozoochory). However, no studies have addressed whether high Considering the worldwide distribution of Cynoglossoideae, diversification rates exhibited by widespread plant groups were its diaspore diversity (unique in the family), and the uneven initially promoted by the acquisition of certain diaspore traits. To diversification within clades, we hypothesize that LDD fruit better elucidate this relationship, new trait- dependent diversifi- specialization resulted in geographic range expansion and an in- cation analyses have been developed. Recently, Larson-Johnson creased rate of diversification. To test this hypothesis, we recon- (2016) has suggested that biotically dispersed lineages of Fagales structed the biogeographic history and morphological evolution display higher diversification rates than abiotically dispersed of fruits across a time- calibrated phylogeny of Cynoglossoideae. ones. Nevertheless, such investigations are still needed for other Specifically, we (1) characterized diaspore functional traits asso- hyperdiverse angiosperm groups. ciated with LDD syndromes using SEM, light microscopy, and The origin of Boraginaceae (105 genera, ~1600 species) has literature sources; (2) reconstructed the evolution of diaspore been dated to the late Cretaceous in Eurasia (Luebert et al., 2017). (typically fruits) syndromes across the phylogeny; and (3) eval- This family is characterized by schizocarpic fruits that split into uated whether diaspore traits related to LDD (epizoochorous) four one- seeded units (although some exceptional species have favored large geographic distributions and high diversification
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