Evolutionary and ecological significance of cryptic diversity in foraminifera: the extent and structure of genetic diversity in planktonic foraminifera
Palaeontology
Final Report Abstract
Planktonic foraminifera are important marine pelagic calcifiers, whose shells accumulate in large quantities on the sea floor and provide a uniquely continuous record of their evolution and of the interplay between their populations and global change in the past. Many applications of planktonic foraminifera in paleoceanography and paleobiology assume that the morphologically defined species of planktonic foraminifera represent biological species with unique niche requirements. Molecular genetic analyses have in the last two decades provided evidence for the existence of a morphologically “cryptic” level of diversity within individual species. These “cryptic” genetic types often show distinct biogeographies, unique ecological adaptations and appear to be of ancient origin. In order to provide an interface between processes at this “cryptic” level of divergence and paleoapplications of planktonic foraminifera, this project investigated a set of key species throughout their global habitat. The aims were to characterize the occurrence and geographical distribution of “cryptic” genetic types, assess the congruence between morphological and molecular taxonomy and verify the taxonomic level of the “cryptic” genetic types by developing new genetic markers. Building on the data, techniques and collections developed during the first phase of this project, in GEDIFORAM II we focused on three key species. By producing large global datasets for these species, we were able to discover novel patterns in their distribution, confirm the existence of habitat segregation among closely related types and indicate that the extent of the genetic diversity within species is limited and can be globally estimated in collections of limited size and geographic extent. In the conspicuous species Hastigerina pelagica, we have discovered a remarkably strong vertical segregation among the nearest related types, which provided the first genetic evidence for the existence of depth-parapatric speciation in marine microplankton. A study of the paleoceanographically important species Globigerinoides sacculifer revealed the absence of genetic diversity within this morphologically diverse taxon. This discovery was most unexpected and questions the traditional assumption that morphological species in planktonic foraminifera corresponds to biological diversity or are at least consistently scaled with it (all morphological species containing multiple “cryptic” species). For the analysis of this species, we have developed new genetic markers that allowed us to confirm the absence of reproductive isolation within the “cryptic” genetic types recognized by previously used markers. This strongly suggests that these “cryptic” species are biological species sensu Mayr. The “cryptic” nature of these genetically defined species may arise from a combination of a decoupling between the rates of genetic and morphological evolution or from the failure of current taxonomic concepts. These are based on characters of the calcite shell and have rarely been tested against independent evidence. An investigation of the species Globigerinoides ruber, initiated during the first phase of the project, revealed a consistent link between shell morphology and genetic relatedness, allowing us to “revive” an abandoned taxonomic concept and clarify the phylogeny of this species. When projected onto the fossil record, the new taxonomy and phylogeny indicates an unexpected evolutionary path, which is entirely consistent with fossil occurrence of the involved species. In the course of this project, we have succeeded in obtaining DNA data from several species that were never sequenced before. The position of these new sequences in phylogenetic trees is congruent with their classification and has little impact on the shape of the tree. Together with the observation that the cryptic genetic diversity is limited, these results suggest that environmental sequencing may be a viable option in the future to characterize the diversity and biogeography of planktonic foraminifera. Such endeavors, as well as attempts to resolve the phylogeny of the group and apply methods of molecular biology to investigations of its physiology require access to new genetic markers and ultimately the entire genome. To this end, we carried out a pilot study in which we generated a large sequence library from specimens that underwent natural reproduction and genome multiplication into gametes. The analysis of this dataset will allow us to direct future studies towards the assembly of the entire genome.
Publications
- (2009). Using the multiple analysis approach to reconstruct phylogenetic relationships among planktonic foraminifera from highly divergent and length polymorphic SSU rDNA sequences. Bioinformatics and Biology Insights, 3, 155–177
Aurahs R, Göker M, Grimm GW, Hemleben V, Hemleben C, Schiebel R, Kucera M
- (2009).Geographic distribution patterns of cryptic genetic types in the planktonic foraminifer Globigerinoides ruber. Molecular Ecology 18, 1692–1706
Aurahs R, Grimm GW, Hemleben V, Hemleben C, Kucera M
- (2010). A Clustering Optimization Strategy for Molecular Taxonomy Applied to Planktonic Foraminifera SSU rDNA. Evolutionary Bioinformatics, 6, 97-112
Göker M, Grimm GW, Auch A, Aurahs R, Kucera M
- (2011). A revised taxonomic and phylogenetic concept for the planktonic foraminifer species Globigerinoides ruber based on molecular and morphometric evidence. Marine Micropaleontology, 79, 1-14
Aurahs R., Treis Y., Darling K.F., Kucera M.
