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

https://doi.org/10.1016/j.envexpbot.2019.103892Get rights and content

Highlights

  • A new concept (´endangered living fossil´) is proposed based on conservation and phylogenetic criteria.

  • Endangered, monspecific genera are good candidates to test whether they are endangered lineages of great evolutionary heritage.

  • California, Chile and Mediterranean Basin provide 11 examples.

  • They help infer causes for extinction and survival postdating historical climate changes.

  • We urge the IUCN to consider evolutionary criteria for species prioritization.

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.

Introduction

The term ‘living fossil’ has historically been used to describe isolated, anomalous species of animals (various examples of cnidarians, sponges, molluscs, brachiopods, insects, pancrustaceans, lungfishes, amphibians, mammals, sauropsids), plants (cycads, conifers), and archaeans (nanoarchaeotans). A quick search in academic databases for the key word ‘living fossil’ in the title of scientific papers rendered 256 publications since 1940 using Scopus (scopus.com), 210 publications since 1953 using Web of Science (clarivate.com/products/web-of-science) and 453 publications since 1971 using Google Scholar (scholar.google.com) (October 2018). Therefore, the use of the term ‘living fossil’ in the last decades indicates that it is still a hot topic in science (Fig. S1). The advent of phylogenetics to reconstruct the evolutionary history of organisms (Ronquist, 2014), new palaeobotanical discoveries (Alroy, 2019 at www.fossilworks.org), and an increasing number of journals (Louys et al., 2017) appear to be responsible for the high number of publications including the term ‘living fossil’. Nevertheless, lack of a clear definition and an explicit hypothesis to be tested has made authors interpret the concept in different, albeit related ways: (i) a species that has no close living relatives (Casane and Laurenti, 2013), (ii) a species or lineage that persists with relatively little morphological change “for a long time” (Yoshida, 2002); (iii) an evolutionary relict of a once large radiation (Nagalingum et al., 2011); (iv) a species that was first discovered in the fossil record and subsequently found to be still extant (Forey, 1984), among others. Therefore, our search found a relatively free usage of the term in publications, which sometimes include ‘living fossil’ only in the title apparently to draw readers’ attention.

The reason behind a relaxed usage of the term is the original description itself. Charles Darwin (1859) coined the concept ‘living fossil’ in a fanciful sense to reflect “anomalous forms” in the Tree of Life (see Vargas and Zardoya, 2014). He used the term twice in On the Origin of Species to discuss the observation of certain organisms that are remarkably different from their closest relatives: (i) “These anomalous forms may almost be called living fossils; they have endured to the present day, from having inhabited a confined area, and from having thus been exposed to less severe competition” (page 122); and (ii) “Species and groups of species, which are called aberrant, and which may fancifully be called living fossils, will aid us in forming a picture of the ancient forms of life” (page 503).

The term ‘living fossil’ has therefore been a contentious subject rather than a clear concept with a single meaning (see Bennett et al., 2018 and references therein). Some authors have tried to solve the problem by proposing the use of ‘relict’ as a related term that is more testable than ‘living fossil’ because the former does not imply maintenance of ancestral characters (Grandcolas et al., 2014). The two terms are not equivalent, but they both put forward essential ideas about the course of evolution for declining organisms that scientists discuss in many evolutionary studies, albeit few quantify them (Bennett et al., 2018). In particular, ‘relict’ implies a remnant of organisms formerly more abundant, while ‘living fossil’ reflects isolation of organisms whose evolutionary lineages are almost extinct (Grandcolas et al., 2014). In other words, the term ‘relict’ also lacks precision. An alternative approach is to consider that both terms are essential evolutionary components that need to be narrowed down for precision by using specific adjectives. Indeed, four concepts of ‘relict’ have already been proposed depending upon the scope of particular studies: geographic, taxonomic, lineage and ancient relicts (Cronk, 1992; Vargas, 2007).

In the present paper we do not aim to give a new definition for ‘living fossil’ given the conceptual problems above indicated. Rather, we use phylogenetic and conservation approaches to propose a more specific concept in biodiversity conservation, namely ‘endangered living fossil’ (ELF). We propose three conditions that an ELF needs to meet: (1) scarcity and narrow distribution, i.e. few populations and localities lead to catalogue the species as either ʻendangered’ or ‘critically endangered’ using IUCN criteria; (2) evolutionary distinctiveness, i.e. phylogenetic singularity of a single-species clade (typically a monospecific genus) as a result of a null rate of diversification; (3) ancient divergence, i.e. an old lineage with a stem age predating the dramatic environmental changes of a particular geological epoch as revealed by time-calibrated phylogenies.

Taking all together, our working hypothesis is that genera that have a single, endangered species each are survivors of the dramatic environmental changes since at least the Miocene-Pliocene boundary. To test this hypothesis, we contrasted time-calibrated phylogenies of vascular plants distributed in the Iberian Peninsula (mainland Spain, mainland Portugal, and the Balearic Islands) in order to assess a pre-Pliocene origin of monospecific genera already catalogued as ‘endangered’ and ‘critically endangered’ by previous IUCN conservation studies. To provide evidence of the validity of this approach, we also tested the ELF concept for the five mediterranean floristic regions of the world.

Section snippets

Material and methods

Conservation of species and lineages should be currently addressed based on spatio-temporal analyses using phylogenetic methods. The spatial approach searches for geographic areas of accumulation of lineages for any flora or fauna (Rosauer et al., 2009; Mishler et al., 2014; Rosauer and Jetz, 2015). The temporal approach focuses on both evolutionary origin (evolutionary distinctiveness) and conservation status (global threat) of taxa for any flora or fauna (Isaac et al., 2007). We herein

Iberian Peninsula and Balearic Islands

Sister-group relationships were supported by PPs>0.90 for all six Iberian genera, and by PPs>0.95 for all but Avellara (PP = 0.92) (Fig. 2a). Estimated tMRCAs of study genera and their sister groups ranged from the late Eocene to the early Pleistocene, with the highest concentration in the Miocene (Fig. 2a, b; Table 1). These results supported an ELF status for Gyrocaryum, Castrilanthemum, Avellara, Gadoria and Naufraga, but not for Pseudomisopates. Phylogenetic relationships and divergence

Discussion

The hypothesis of ELFs was successfully assessed for 18 endangered, monospecific genera (six from the Iberian Peninsula and 12 from other areas of the five MFRs) of the 28 initially chosen. In particular, 11 of them from three (California, Chile and Mediterranean Basin) of the five MFRs of the world showed to be ELFs. We failed to analyse ten more genera because of lack of time-calibrated phylogenetic data. Therefore, the hypothesis of ancient divergence (pre-Pliocene) is supported for 11

Conclusions

The ‘endangered living fossil’ (ELF) concept stems from the combination of taxonomic, phylogenetic and conservation principles. Comparison among floras that share similar climatic conditions, such as the summer drought that is characteristic of mediterranean climates, may shed light on causes of extinction and survival of lineages facing dramatic climate changes. We argue that ELF is a testable concept based on criteria that can be additionally applied not only to other floras of the world but

Author contribution statement

All authors contributed equally.

Declaration of Competing Interest

We declare no conflict of interests.

Acknowledgements

The authors thank Ana Otero and Salvatore Tomasello for providing phylogenetic datasets. M.F.-M. was supported by a Juan de la Cierva fellowship (Spanish Ministry of Economy, Industry and Competitiveness, reference IJCI-2015-23459). This research was funded by Banco Santander, the Spanish National Research Council (CSIC) and Fundación General CSIC (FGCSIC) through a Proyecto Cero on endangered species 2010 (‘Do all endangered species hold the same value?: origin and conservation of living

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