Palaeobiodiversity and taxonomic resolution: linking past trends with present patterns

Authors


The relevance of palaeobiodiversity studies and of the applications of these studies to general biological and conservation topics is increasing. This trend is due in part to the attainment of sufficient temporal resolution, thus reducing the gap and increasing the continuity between palaeoecological data series and present-day observations (Hughes & Ammann, 2009). Problems of taxonomic resolution, however, still hamper the complete integration of past records into current biological research. This topic is the focus of the present discussion, which addresses the record of past trends in biodiversity and aims to act as a warning call for both palaeobiologists and biologists working on extant species. These concerns are raised in relation to the reliability of conclusions based on palaeodiversity studies as a function of the taxonomic resolution of such studies. Potential solutions to the problem are also proposed. Emphasis is placed on extant biodiversity patterns, particularly the latitudinal diversity gradients (LDG), whose origin and potential drivers are currently being debated using palaeoecological and molecular phylogenetic tools, and on biodiversity conservation, a highly topical issue.

Present-day biodiversity has been defined on the basis of species and on subspecific categories with sufficient amounts of genetic difference to warrant consideration as evolutionarily significant units (ESUs), the lower taxonomic unit needed to represent the actual genetic variability associated with a distinct evolutionary potential. ESUs are also a preferred category for biodiversity conservation purposes (Moritz, 1994). Under this framework, genera and higher taxonomic categories are not suitable biodiversity indicators. The difficulty associated with such taxa is that they may contain a wide range of internal diversity, from one to a thousand or more species. From a palaeoecological point of view, species are effective indicators in relation to ecological and environmental features, whereas higher taxonomic categories represent imperfect proxies and compromise the reliability of palaeoecological reconstructions (Birks & Birks, 1980). A partial solution has been the use of characteristic and recurrent fossil assemblages as proxies for communities and, therefore, for a range of known ecological conditions. However, both the realization that species respond individually to environmental changes and the resulting lack of modern analogues for many fossil assemblages (Jackson & Williams, 2004) serve to bring in to focus the issue of insufficient taxonomic resolution.

Palaeoecology is more constrained than molecular phylogenetics as a tool for taxonomic resolution because fossil and sub-fossil identification is mostly based on morphological characters. These characters are often insufficient for accurate biodiversity reconstruction at the species level. Additional issues include the problem of differential preservation and the difficulty that, in several cases, the number of preserved fossils does not correspond to the number of individuals of the parent species. The latter difficulty occurs, for example, with pollen, seeds or leaves. The most favourable situation corresponds to organisms whose preserved parts are diagnostic at the species level and for which the number of original individuals coincides with or can be reliably estimated from the number of preserved fossils, as is the case for diatom frustules or foraminiferal linings. The confidence associated with palaeobiodiversity estimates also depends on the time interval considered. This level of confidence is maximal in the Quaternary, where a higher number of fossils can be assigned to extant species through morphological comparisons, and it decreases progressively in earlier times, for which only comparisons at supraspecific levels are possible. In certain cases, the affinities of the study material with modern taxa are wholly unknown, especially in the case of extinct species, and fossils are classified into morphospecies to allow them to be catalogued in the hope that further studies will shed light on their phylogenetic affinities. Several attempts have been made to quantitatively relate fossil biodiversity to actual biodiversity. The case of pollen is especially difficult because factors such as differential pollen production, dispersal and sedimentation primarily influence the resulting pollen assemblage. A sound relationship between past plant diversity and its derived pollen richness is still elusive (van der Knaap, 2009).

Palynology is one of the more widely used methods of palaeoecological reconstruction. As a result, the difficulty of deriving confident estimates of past diversity undermines our ability to identify potential environmental forcing agents. However, a recent study by Connor et al. (2012) in the Azores archipelago using diversity estimates based on pollen accumulation rates (PAR), instead of percentages, shows that palaeodiversity trends are consistent with ecological changes linked to human arrival and further activities. The main lesson is that, although pollen diversity is not a direct proxy for plant diversity, the trends in both pollen and plant diversity may show parallelisms useful for palaeoecological inference. To date, studies on past biodiversity shifts and their possible causes have been performed by attaining the maximum resolution possible using morphological comparison. A more accurate taxonomic approach is needed to strengthen the links between past and present-day observations as well as to derive confident predictions for the future. The main contribution of palaeoecology in the present context has been the identification of potential environmental agents (drivers) of past diversification trends.

Conversely, DNA molecular phylogenetics has an enormous potential for taxonomic resolution at the ESU level, but this potential is not always fully exploited. During recent decades, such studies have effectively addressed the issue of the origin of higher tropical diversity, but their conclusions differ according to the taxonomic level used. An example of the different interpretations that can be derived from generic and ESU approaches is furnished by recent studies of the Neotropics. A meta-analysis based on the molecular dating of the initial speciation stages within the present-day Amazon Basin genera or crown dating, which coincides with the age of the oldest extant species of each genus but ignores the age of origin of younger species, suggests that the extant Neotropical biodiversity was already attained by the early Miocene [c. 20 million years ago (Ma)]. This analysis suggests that the primary agent of diversification is the Andean orogeny and its associated palaeogeographic rearrangements (Hoorn et al., 2010). Conversely, other meta-analyses that consider the age of origin of every individual living ESU (species dating) show that speciation has been more or less continuous, without apparent bursts, since the beginning of the Miocene (c. 25 Ma) until the Quaternary [the last 2.6 million years (Myr)] (Rull, 2011). Therefore, Neotropical diversification is viewed as a more complex process, in which both Mio-Pliocene (c. 25–5 Ma) palaeotopographic/palaeogeographic reorganizations and Pliocene–Quaternary (the last c. 5 Myr) climatic changes have had a significant role (Rull, 2011). Crown dating is useful when dealing with the ancestors of present-day species, but species dating is preferred if extant ESUs represent the target of the investigation.

To find solutions in the future, it is clear that the taxonomic potential of molecular phylogenetics should be fully exploited to maximize the interpretative capabilities of this approach. This task is not especially difficult. It depends primarily on the identification of appropriate DNA markers and a representative sampling of the extant ESU under study as well as a suitable chronological calibration. In the case of palaeoecology, however, the associated handicaps are still significant for the reasons stated above. Fortunately, several recent advances may serve to improve this situation. The identification of fossils and organic remains would benefit greatly from the rapid development of molecular genetic techniques, but the applicability of these techniques is hindered by the availability of intracellular material, including preserved ancient DNA. Successful experiences in this context are already available in Quaternary studies using bones, eggs, amber, seeds or pollen, among others (Anderson-Carpenter et al., 2011). These structures provide physical protection that facilitates DNA preservation, but studies on extracellular sedimentary DNA have also been attempted in both marine and freshwater sediments, as well as in the permafrost (Hofreiter et al., 2012). The need for well-preserved genetic material and the possibility of linking DNA remains with extant species restrict the utility of these methods to relatively recent Neogene and Quaternary times. However, this time-scale is of general relevance because most extant species whose origin has been dated by molecular phylogenetic methods are known to have emerged during the last c. 25 Myr (Miocene to Quaternary).

In summary, studies aimed to link Neogene–Quaternary trends and present patterns of biodiversity should combine both palaeoecology and molecular phylogenetics and should place emphasis on ESUs and their identification, rather than on higher taxonomic categories. This approach appears to be the best way to understand present-day biodiversity patterns in the light of the past processes that generated them. In addition, it represents the most reliable mode available to forecast potential future diversity trends under the predicted environmental changes. This observation implies that palaeoecologists should be attentive to new developments in molecular phylogenetics and other palaeogenetic techniques useful for identifying fossils and subfossils at the species and ESU levels. Promising tools have been cited in this discussion, but new ones are to be anticipated in the future. Biologists working on present-day organisms should in the meantime exercise caution in palaeodiversity studies based on genera and higher taxonomic categories, especially if their results have implications for the understanding of present-day biodiversity patterns.

Editor: John Lambshead

Ancillary