Phylogenetic analysis of fossil flowers using an angiosperm-wide data set: proof-of-concept and challenges ahead

Abstract

Premise: Significant paleobotanical discoveries in recent decades have considerably improved our understanding of the early evolution of angiosperms and their flowers. However, our ability to test the systematic placement of fossil flowers on the basis of phylogenetic analyses has remained limited, mainly due to the lack of an adequate, angiosperm-wide morphological data set for extant taxa. Earlier attempts to place fossil flowers phylogenetically were, therefore, forced to make prior qualitative assessments of the potential systematic position of fossils and to restrict phylogenetic analyses to selected angiosperm subgroups.

Methods: We conduct angiosperm-wide molecular backbone analyses of 10 fossil flower taxa selected from the Cretaceous record. Our analyses make use of a floral trait data set built within the framework of the eFLOWER initiative. We provide an updated version of this data set containing data for 28 floral and two pollen traits for 792 extant species representing 372 angiosperm families.

Results: We find that some fossils are placed congruently with earlier hypotheses while others are found in positions that had not been suggested previously. A few take up equivocal positions, including the stem branches of large clades.

Conclusions: Our study provides an objective approach to test for the phylogenetic position of fossil flowers across angiosperms. Such analyses may provide a complementary tool for paleobotanical studies, allowing for a more comprehensive understanding of fossil phylogenetic relationships in angiosperms. Ongoing work focused on extending the sampling of extant taxa and the number of floral traits will further improve the applicability and accuracy of our approach.

Keywords: angiosperms; eFLOWER; floral evolution; floral structure; fossil flowers; mesofossils; molecular backbone; phylogenetic analysis.

FIGURE 1

Results for Chloranthistemon endressii from angiosperm‐wide molecular backbone analyses using maximum parsimony, based on 12 floral characters that could be scored for this fossil (of 30 secondary characters in the data set). The backbone tree (circular chronogram) is a transformed version of the maximum clade credibility tree from Magallón et al. (2015), and the floral morphological data set for the 792 extant taxa is an updated version of the data set from Sauquet et al. (2017). Black branches in trees (circular tree and scaled‐up partial tree on the right) indicate most parsimonious (MP) positions; green branches indicate positions that are one step less parsimonious (MP+1). A gradient from yellow to gray branches indicates positions three or more steps less parsimonious. The same color coding applies to the legend in the lower left, indicating the number of most and less parsimonious positions. The drawing in the lower right shows the three‐lobed androecium of C. endressii (reproduced from Friis et al., 2011, with permission of Cambridge University Press). The position of Chloranthaceae is indicated by an orange bar in the circular chronogram. The concentric circles superimposed on the chronogram indicate a time scale with intervals of 20 million years, with the age of the most recent common ancestor of all angiosperms in the center of the figure set to 139.4 million years according to Magallón et al. (2015). The pink circle indicates the approximate age of C. endressii according to Crane et al. (1989).

FIGURE 2

Results for Dakotanthus cordiformis from angiosperm‐wide molecular backbone analyses using maximum parsimony, based on 29 floral characters that could be scored for this fossil. The color coding, the time scale superimposed on the circular chronogram, and the sources of the backbone tree and morphological data set of extant taxa are as in Figure 1. The drawing in the lower right shows the pentamerous flower of D. cordiformis (reproduced from Manchester et al., 2018, with permission of De Gruyter). The position of the order Fabales is indicated by an orange bar in the circular chronogram. The pink circle indicates the approximate age of D. cordiformis according to Manchester et al. (2018).

FIGURE 3

Results for Microvictoria svitkoana from angiosperm‐wide molecular backbone analyses using maximum parsimony, based on 20 floral characters that could be scored for this fossil. The color coding, the time scale superimposed on the circular chronogram, and the sources of the backbone tree and morphological data set of extant taxa are as in Figure 1. The drawing in the lower right shows a reconstruction of the complex flowers of M. svitkoana (reproduced from Crepet et al., 2004, with permission of Wiley). The positions of the ANA grade (Amborellales, Nymphaeales, and Austrobaileyales) and of Calycanthaceae (Laurales), respectively, are indicated by orange bars in the circular chronogram. The pink circle indicates the approximate age of M. svitkoana according to Gandolfo et al. (2004).

FIGURE 4

Results for Spanomera mauldinensis from angiosperm‐wide molecular backbone analyses using maximum parsimony, based on 25 floral characters that could be scored for this fossil. The color coding, the time scale superimposed on the circular chronogram, and the sources of the backbone tree and morphological data set of extant taxa are as in Figure 1. The drawing in the lower right shows a female and a male flower of S. mauldinensis (reproduced from Friis et al., 2006, with permission of Elsevier). The position of the Gunnerales and Buxales is indicated by an orange bar in the circular chronogram. The pink circle indicates the approximate age of S. mauldinensis according to Drinnan et al. (1991).