‘Endangered living fossils’ (ELFs): Long-term survivors through periods of dramatic climate change

Abstract

Geography and climate have been the main drivers of evolution in recent geological epochs. While new lineages of species have been formed in the last millions of years (speciation) and others have vanished as a result of historical climate changes (extinction), some ancient lineages appear to have persisted to the present day without net diversification. In this paper, evolution of ancient lineages is addressed by combining phylogenetic and conservation approaches to test the concept of ‘endangered living fossil’ (ELF). Using endangered, monospecific genera as starting point, we propose three criteria to identify ELFs (in order): (1) scarcity and narrow distribution of populations, i.e. the species (and thus the genus) is categorised as either ‘endangered’ or ‘critically endangered’ using IUCN criteria; (2) evolutionary distinctiveness, i.e. phylogenetic singularity of a single-species lineage as a result of a null net diversification rate; (iii) ancient divergence, i.e. split from the closest extant relatives predating the dramatic climate changes of particular geological epochs (specifically changes since the Miocene-Pliocene boundary). The vascular flora of the Iberian Peninsula offers a suitable study system to reliably test the ELF concept. Indeed, time-calibrated phylogenies revealed that five of the six critically endangered, monospecific genera endemic to the Iberian Peninsula are ELFs. These five genera appear to have diverged from their closest relatives in the Oligocene (Gyrocaryum), Miocene (Avellara, Castrilanthemum, Gadoria) and around the Miocene-Pliocene boundary (Naufraga). This result entails long-term survival (with no net diversification) through at least three dramatic climate changes: the Messinian Salinity Crisis (late Miocene), the establishment of the mediterranean climate (Pliocene), and the glacial-interglacial cycles (Pleistocene). Using results from the literature, we found examples of ELFs for the mediterranean floras of California (Dodecahema), Chile (Avellanita, Gomortega, Legrandia) and other Mediterranean areas of Europe (Petagnaea, Phitosia). ELFs are unique and threatened lineages representing an exceptional evolutionary heritage, and therefore they should be prioritised in biodiversity research and conservation programs.