Review papersFossil record of the Icacinaceae and its paleogeographic implications
Introduction
In the past decades, the concept of Icacinaceae has been revised considerably with the results of new molecular and morphological data that show that the former Icacinaceae family concept with about 400 species and 58 genera (from Sleumer, 1942) was polyphyletic (Kårehed, 2001). That phylogenetic study defined the Icacinaceae s.s. as belonging to the Garryales order and placed some genera in the Aquifoliales and Apiales orders. In particular, Kårehed described a new family, Stemonuraceae, and added some species to the Cardiopteridaceae family. The resulting circumscription of Icacinaceae included only 36 genera divided in four informal groups: Icacina, Cassinopsis, Emmotum, and Apodytes. Later, another study showed that this new circumscription of Icacinaceae corresponds to a basal lamiid group (Lens et al., 2008). According to Lens et al. (2008), the Icacinaceae have simple perforation plates in vessels (except for Cassinopsis), which is not the case for other excluded former Icacinaceae. However, Icacinaceae (sensu Lens et al., 2008) was still considered as a polyphyletic group (Byng et al., 2014). More recently, a new Icacinaceae s.s. family was delimited with only the Icacina group sensu Kårehed (2001) accepted, using a new molecular data set (Stull et al., 2015). Icacinaceae s.s. (sensu Stull et al., 2015) contains only 23 genera, with about 160 species, and is a basal lamiid group close to the Oncothecaceae family. Both families are in the newly defined Icacinales order. Those taxonomic assignments are accepted and used in the APG IV (APG, 2016). Thus, the Icacinaceae family s.l. belongs now to four indirectly related orders in Asterids group (Fig. 1).
This family possesses an extensive fossil record that extends geographically and geologically. The record is mainly composed of endocarps (e.g., Reid and Chandler, 1933, Manchester, 1994, Collinson et al., 2012) but there are also reports of wood (e.g., Greguss, 1969), pollen (e.g., Kedves, 1970, Krutzsch and Vanhoorne, 1977, Cavagnetto, 2000), a flower (Del Rio et al., 2017) and leaf remains (e.g., Wolfe, 1977, Tanai, 1990). However, most of the paleobotanical discoveries and descriptions on Icacinaceae family were made before the twenty-first century. Therefore, assignments to Icacinaceae were done before the recent modifications of the phylogenetic framework and some characters used to define Icacinaceae can be in fact been simply apomorphic for Asterids (Fig. 1).
Some fossil species (e.g., Icacinoxylon alternipuncata, Icacinicarya papillaris, and Iodes germanica), were used to calibrate an angiosperm phylogeny (Magallón et al., 2015). In addition, the Icacinaceae fossil remains have been used as a paleoclimatic clue and contributed to the characterization of the Boreotropical forest definition, a vegetation type that was widespread across middle latitudes in Northern Hemisphere during the Eocene (Wolfe, 1975). The Icacinaceae fossils also played an important role in the understanding of the dispersion between Europe and North America during the early-middle Eocene (Manchester, 1994, Stull et al., 2011, Allen et al., 2015). Thus, it is crucial to evaluate the Icacinaceae fossil record within a phylogenetic framework. Two reviews of the fossil record including the asteridae were made (Martínez-Millán, 2010, Manchester et al., 2015), highlighting a Maastrichtian minimum age for the Icacinaceae family. However, neither of these reviews embraces all the Icacinaceae fossils described until now.
In this study, we reviewed previously published reports of fossils attributed to the Icacinaceae. Our main questions are: (1) what is the fossil diversity of Icacinaceae s.s. following the new circumscription of the family and (2) what is the paleogeography and biogeographic history of this family based on this new circumscription?
Section snippets
Material and methods
We compiled all the occurrences of Icacinaceae in the literature to the extent of our knowledge (Table 1.). The fossil record depends on available outcrops, search efforts, and findings. Here we took into consideration a majority of species from North America and Europe. This distribution is probably due to a more thorough search effort in this area than others in paleobotanical history (Morley and Dick, 2003). Indeed, Icacinaceae fossils were recently found from Paleocene–Miocene range in
Species and occurrences rejected or dubious
The endocarp record is the most meaningful for the Icacinaceae family, and probably the most reliable. However, some occurrences need to be revisited.
Comicilabium atkinsii was considered as belonging to Icacinaceae by its unilocular endocarp, the vascular bundle on only one side and the cellular structure of the endocarp wall (Manchester, 1994). The endocarp apical structure is a bulge with a lip. The size of the endocarp and the wall thickness (2–4 mm) are surprising for an Icacinaceae
Age of the family
The age of Icacinaceae was estimated at 96.7 Ma with the help of molecular phylogeny (Magallón and Castillo, 2009). In another recent study, the estimated age was 104 Ma (Wikström et al., 2015). This analysis used 17 fossil calibration points, but these are from various asterids, no Icacinaceae fossil records were included. In another molecular study, the estimated age is between 103 and 110 Ma, with the maximum likelihood method and between 65.5 and 100.3 Ma with a Bayesian analysis (Magallón
Conclusion
Among the 183 occurrences previously described as Icacinaceae, only 92 were accepted as belonging to this family in this study and are mainly from endocarp remains. The minimum age of the Icacinaceae family is probably the Upper Maastrichtian given by the fossil record for the Icacinaceae family. With the accepted samplings, we show an increase of the species richness during the Paleocene, probably due to the increase of temperature during the Thanetian. A great increase of diversity in term of
Author Contributions
DDF designed the project, CDR did the references work, CDR & DDF wrote the manuscript and the discussion part.
Declaration of Competing Interest
None
Acknowledgments
This work was supported by a grant from Agence Nationale de la Recherche under the LabEx ANR-10-LABX-0003-BCDiv, in the program “Investissements d'avenir” n_ ANR-11-IDEX-0004-02 and by the CR2P (UMR 7207).
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