A Rich Fossil Record Yields Calibrated Phylogeny for Acanthaceae (Lamiales) and Evidence for Marked Biases in Timing and Directionality of Intercontinental Disjunctions

Abstract

More than a decade of phylogenetic research has yielded a well-sampled, strongly supported hypothesis of relationships within the large ( > 4000 species) plant family Acanthaceae. This hypothesis points to intriguing biogeographic patterns and asymmetries in sister clade diversity but, absent a time-calibrated estimate for this evolutionary history, these patterns have remained unexplored. Here, we reconstruct divergence times within Acanthaceae using fossils as calibration points and experimenting with both fossil selection and effects of invoking a maximum age prior related to the origin of Eudicots. Contrary to earlier reports of a paucity of fossils of Lamiales (an order of ∼ 23,000 species that includes Acanthaceae) and to the expectation that a largely herbaceous to soft-wooded and tropical lineage would have few fossils, we recovered 51 reports of fossil Acanthaceae. Rigorous evaluation of these for accurate identification, quality of age assessment and utility in dating yielded eight fossils judged to merit inclusion in analyses. With nearly 10 kb of DNA sequence data, we used two sets of fossils as constraints to reconstruct divergence times. We demonstrate differences in age estimates depending on fossil selection and that enforcement of maximum age priors substantially alters estimated clade ages, especially in analyses that utilize a smaller rather than larger set of fossils. Our results suggest that long-distance dispersal events explain present-day distributions better than do Gondwanan or northern land bridge hypotheses. This biogeographical conclusion is for the most part robust to alternative calibration schemes. Our data support a minimum of 13 Old World (OW) to New World (NW) dispersal events but, intriguingly, only one in the reverse direction. Eleven of these 13 were among Acanthaceae s.s., which comprises > 90% of species diversity in the family. Remarkably, if minimum age estimates approximate true history, these 11 events occurred within the last ∼ 20 myr even though Acanthaceae s.s is over 3 times as old. A simulation study confirmed that these dispersal events were significantly skewed toward the present and not simply a chance occurrence. Finally, we review reports of fossils that have been assigned to Acanthaceae that are substantially older than the lower Cretaceous estimate for Angiosperms as a whole (i.e., the general consensus that has resulted from several recent dating and fossil-based studies in plants). This is the first study to reconstruct divergence times among clades of Acanthaceae and sets the stage for comparative evolutionary research in this and related families that have until now been thought to have extremely poor fossil resources.

Shifts in diversification rates linked to biogeographic movement into new areas: An example of a recent radiation in the Andes

“…At this point, we cannot accept or reject any of the biogeographic hypotheses described-the two stepwise migrations through North America or the long-distance dispersal from the Mediterranean climatic region-which highlights the diffi culty of inferring ancestral colonization routes even when using modern ancestral range reconstruction methods (see Tripp and McDade, 2014 ), especially with a non-existent fossil record.…”

Acanthaceae da Marambaia, Estado do Rio de Janeiro, Brasil

“…As Acanthaceae são elementos comuns no subbosque de vegetações tropicais (Tripp & McDade 2014, sendo importantes elementos na manutenção da fauna polinizadora por reunir espécies exclusivamente polinizadas por animais (zoófilas) (Judd et al 2008. Além de ocuparem diferentes substratos, a enorme variedade de formas, cores e dimensões das flores e inflorescências permite uma vasta gama de polinizadores e uma revisão sobre os visitantes das flores de Acanthaceae é apresentada por Matias & Consolaro (2015).…”

“…As Acanthaceae reúnem cerca de 200 gêneros e pelo menos 4000 espécies, estando dentre as dez famílias mais numerosas das plantas com flores , Tripp & McDade 2014, Daniel & McDade 2014. Exceto pela beleza de algumas espécies ornamentais (Lorenzi & Souza 2008, Sartin et al 2014, Tripp & McDade 2014, em função da grande variação morfológica e de classificações baseadas em aspectos de difícil reconhecimento, foram pouco estudadas no século passado.…”

“…Exceto pela beleza de algumas espécies ornamentais (Lorenzi & Souza 2008, Sartin et al 2014, Tripp & McDade 2014, em função da grande variação morfológica e de classificações baseadas em aspectos de difícil reconhecimento, foram pouco estudadas no século passado. Atualmente, o entendimento da família tem se tornado conciso e sua sistemática elucidada com base na filogenia molecular (e.g., Schwarzbach & McDade 2002, McDade et al 2005, 2008, Borg et al 2008, Daniel & McDade 2014, entre outros) e na taxonomia formal (e.g., Wasshausen 1995, Wasshausen & Wood 2004, Scotland & Vollesen 2000, Ezcurra 1993, 2002, Kameyama 2008.…”

Genome-scale transcriptional study of hybrid effects and regulatory divergence in an F1 hybrid Ruellia (Wild Petunias: Acanthaceae) and its parents

“…These two species were selected for the present study first because we were particularly interested in transgressive effects that arise from the union of divergent (vs. closely related) genomes. Ruellia elegans and R. speciosa belong to two different lineages within the genus, whose stem groups are separated by at least 1 million years [31]. Second, these species are important from both economic and scientific perspectives: whereas Ruellia elegans is widely cultivated in the horticultural industry, a complete draft of the nuclear genome of R. speciosa was recently completed, represented only the third family of Asterids with a reference genome sequence [32].…”