Fossilized records of past seas Chris Wade & Kate Darling The planktonic foraminifera (Fig. 1) are Gglobally distributed across the world’s oceans, forming an important part of the zooplankton. The calcitic shells of this fascinating group of organisms are readily preserved in the ocean sediments as micro- fossils (Fig. 2). They form one of the most complete fossil records on earth, stretching across some 130 million years. The record is used to date sedimentary rocks and study evolutionary processes, and is one of the most important archives of past climate. The species, abundance and shape of shells are used to reconstruct sea surface temperatures. Environmental parameters can also be deduced from the chemical composition of the shells. The planktonic foraminifera are therefore used extensively as indicators of climate change. With the advent of molecular biological techniques, it has become possible to study the evolutionary relationships between species of planktonic foraminifera living in the oceans today. These studies have led to the discovery of previously unrecognized genetic diversity, providing the potential to enhance the role of the foraminifera. As well as planktonic forms, there are ABOVE: foraminifera as indicators of past climate. Furthermore, benthic species that live on the ocean floor. The Fig. 1. The planktonic foraminiferan Globigerinoides in combination with their fossil record, planktonic evolutionary transition between benthic and planktonic sacculifer. The cell is enclosed foraminifers provide a unique and ideal tool for forms is of considerable interest. Planktonic species first within a calcitic shell, which has addressing important questions regarding the appear in the fossil record long after the benthic forms, a series of interconnecting mechanisms of plankton speciation and evolution and arose from the adaptation of a benthic species to chambers. This species has an through time. life in the plankton. Since this has been considered to array of spines that serve as a ‘net’ for snaring prey. Energy is be a major evolutionary step, it was concluded that also generated by photosynthesis Origins of the foraminifera all planktonic species arose from a single benthic and this species contains a large It is possible to discover the evolutionary relationships ancestor. This hypothesis is not supported by the number of algal symbionts, which among organisms by comparing their DNA sequences. genetic data; instead of the planktonic species clustering are distributed out along the These relationships are typically shown in the form of spines to maximize light. in a single group, they occupy three separate locations COURTESY DR K. DARLING, an evolutionary tree (a phylogeny). To date, most studies in the molecular tree (Fig. 4), suggesting that the DEPARTMENT OF GEOLOGY AND of the foraminifera have focused on comparing the planktonic way of life has evolved from at least three GEOPHYSICS/ICAPB, UNIVERSITY OF ribosomal (r)RNA genes. When their small subunit independent benthic lines. The planktonic spinose EDINBURGH (SSU) rRNA genes are compared with those of other species (foraminiferans with spines) cluster separately BELOW: eukaryotes, they seem to form one of the earliest from the planktonic non-spinose species, which are Fig. 2. A microfossil of diverging eukaryote lineages in the ‘tree of life’ (Fig. 3). located in two separate regions of the benthic cluster. the planktonic foraminiferan This placement is interesting because it means that the Neogloboquadrina pachyderma, foraminifera could provide information about events Hidden diversity and the implications for obtained from marine sediments. early in eukaryote evolution. However, more work is reconstructing past climate COURTESY DR M. KUCERA, DEPARTMENT OF GEOLOGY, ROYAL needed because the foraminifera show an exceptionally The planktonic foraminifera are divided into HOLLOWAY, UNIVERSITY OF LONDON fast rate of evolution in their rRNA genes. distinct types (‘morphospecies’) based upon Lineages with high rates of evolution the morphology of their shells. One of are notoriously difficult to place in the most interesting outcomes of evolutionary trees, and it has been genetic studies concerns the extent suggested that the foraminifera may of differentiation within these in fact have a far less ancient origin. morphospecies. Most of them show an exceptionally high level From ocean floor to of genetic diversity in their SSU planktonic life rRNA genes, and many include Despite the reservations about more than one genetically distinct external relationships, studies of entity (Fig. 5). Some of these foraminiferal SSU rRNA genes have genetic types may warrant class- provided a great deal of information ification as separate ‘cryptic’ species. about evolutionary relationships within the This finding is important because of the role MICROBIOLOGY TODAY VOL 29/NOV 02 183 of foraminiferal micro- Seas (Fig. 5), and also in individuals from the Trypanosomes Eukaryota fossils in reconstructing Eastern Pacific and Mediterranean in O. universa (Fig. 5). Foraminifera Euglena Acellular slime mould past climates. For climate These findings are important because they suggest Diplomonads Vahlkampfid amoeba reconstruction it has that gene flow is occurring on a global scale, with 100% Dysentry amoeba been assumed that each genetic intermixing between populations as far apart as Tritrichomonads Cellular slime mould morphospecies is a single the Arctic and Antarctic, or the Pacific and Atlantic. Microsporidia entity with a specific This is at odds with the observation that many ecological (and thus morphospecies have high levels of genetic diversity climatic) preference. If and include more than one genetically distinct entity. Eukaryote the distinct genetic types For diversity to arise, it is generally considered that Archaebacteria Crown Group within morphospecies there must be some form of barrier to gene flow. It is are in fact adapted to therefore unclear how diversity arose in the planktonic 10 changes per 100 nucleotide positions different habitats, and foraminifera when there are apparently no effective exhibit different ecological barriers to gene flow. The planktonic foraminifera Eubacteria and climate preferences, raise intriguing questions concerning the process of then the assumption that speciation in the oceans. Caribbean each morphospecies is 98% Caribbean 98% Coral Sea Globigerinella siphonifera Globigerinella siphonifera Southern California Bight characteristic of a par- Southern California Bight 95% Caribbean Orbulina universa ticular climate would be 95% Coral Sea Southern California Bight Orbulina universa 100% Globigerinoides sacculifer wrong. If this is so, there Mediterranean 85% 100% Caribbean Coral Sea Globigerinoides sacculifer 99% Globigerinoides ruber/conglobatus may be significant errors Caribbean Coral Sea 99% Caribbean in current models of Southern California Bight Globigerinoides ruber/conglobatus cluster foraminifera Caribbean 59% 100% Globigerina bulloides climate reconstruction. 85% Coral Sea 93% Spinose planktonic Arctic 100% Turborotalita quinqueloba Antarctic Recent work suggests Antarctic Ammonia 85% 72% Southern California Bight Globigerina bulloides Elphidium that different genetic 100% Arctic Archaias Spinose planktonic foraminifera Antarctic Peneroplis 59% 93% Coral Sea Quinqueloculina types are indeed associated 95% Arctic 72% Massilina Antarctic 95% Neogloboquadrina 100% Arctic Turborotalita quinqueloba with different environ- 72% Antarctic Globigerinita glutinata Coral Sea Bigenerina ments. If it does become non-spinose planktonic foraminifera Bolivina 100% N. pachyderma (Arctic) Textularia N. pachyderma (Antarctic) Neogloboquadrina non-spinose planktonic Trochammina possible to distinguish foraminifera and 72% N. dutertrei (Caribbean) Haynesina Globigerinita glutinata Glabratella 5 changes per 100 nucleotide positions these newly recognized and Astorhiza 5 changes per 100 nucleotide positions Astrammina Allogromia genetic types in the fossil Benthic record, the role of the Benthic ABOVE TOP: foraminifera as indicators of past climate could be greatly Fig. 3. Evolutionary tree showing enhanced. the origins of the planktonic ଙ foraminifera. The eukaryote crown group includes all multicellular Global gene flow and the implications for eukaryotes (including plants, the origin of new species ଙ ଙ animals and fungi) and several Genetic studies of the planktonic foraminifera have ଙ other groups of unicellular protists. also begun to illuminate the processes of speciation in Percentages indicate the level of support for branches in the tree. the oceans. Despite the high degree of genetic ଙ diversity observed in their SSU rRNA genes, identical ABOVE BOTTOM: sequence types (genotypes) have been found in Fig. 4. Evolutionary tree showing individuals collected at opposite ends of the globe in the relationship between planktonic ଙ (red and orange) and benthic several morphospecies (white boxes, Fig. 5). Perhaps foraminifera (blue). The planktonic most remarkable is the discovery of identical rRNA species can be further subdivided genotypes in individuals collected from the Arctic Dr Christopher Wade is a lecturer in Genetics at into species with spines (spinose; and Antarctic subpolar regions within each of the cool- the University of Nottingham, UK. red) and those without spines water morphospecies Globigerina bulloides, Turboratalita Tel. 0115 970 9405; fax 015 970 9906 (non-spinose; orange). Percentages indicate the level of quinqueloba