Micropalaeontology evolution and biodiversity

Micropalaeontology brings three unique perspectives to the study of evolution: the dimension of time, abundance of specimens (allowing statistical analysis of trends) and long complete fossil records, particularly in marine groups. Despite these features giving special insights into the nature of evolutionary processes, micropalaeontologists have until recently concentrated mainly on documenting the ascent of evolutionary lineages, such are described in the separate chapters in this book.

Micro- and macroevolution are the two main modes of evolution. Microevolution describes small-scale changes within species, particularly the origin of new species. Speciation occurs as the result of anagenesis (gradual shifts in morphology through time) or cladogenesis, rapid splitting of a pre-existing lineage. Which of these is the dominant mode has remained one of the most controversial questions in palaeobio-logy in the last 30 years.

Some of the best recorded examples of anagenesis have been documented in planktonic foraminifera (Malmgren & Kennett 1981; Lohmann & Malmgren 1983; Malmgren et al. 1983; Hunter et al. 1987; Malmgren & Berggren 1987; Norris et al. 1996; Kucera & Malmgren 1998), whilst examples of cladogenesis (e.g. Wei & Kennett 1988; Lazarus et al. 1995; Malmgren et al. 1996) are less widely cited. Similar studies have been conducted on Radiolaria (Lazarus 1983, 1986) and diatoms (Sorhannus 1990a, 1990b). Where morphological change has been mapped onto an ecological gradient (such as temperature/depth gradients measured by oxygen isotope analysis) it appears that gradual morphological trends do not strictly reflect the rate of speciation or its mode. For example, Kucera & Malmgren (1998) showed that gradual change in the Cretaceous planktonic foramin-ifera Contusotruncana fornicata probably resulted in a shift in the relative proportion of high conical to low conical forms through time. High conical forms evolved rapidly and gradually replaced the low conical morphs, though at any one time the abundances of different morphs were normally distributed. Similarly, Norris et al. (1996) documented a gradual shift in the average morphology of Fohsella fohshi over ~400 kyr, suggesting only one taxon was present at any given time (Fig. 2.1), yet isotopic data indicated a rapid separation of the population, into surface- and thermocline-dwelling populations and reproductive isolation midway through the anagenetic trend. During the same interval keeled individuals gradually replaced unkeeled forms, a clear example of both anagenesis and clado-genesis occurring in the same population. Another 'classic' example of anagenetic change, that of Glob-orotalia plesiotumida and the descendant G. tumida (Malmgren et al. 1983, 1984), has been challenged by Norris (2000). G. plesiotumida ranges well into the range of G. tumida (e.g. Chaisson & Leckie 1993; Chaisson & Pearson 1997) and therefore cannot have given rise to G. tumida by the complete replacement of the ancestor population. An alternative explanation to this and probably all examples of anagenetic trends is that clado-genesis is quickly followed by a rapid change in the relative proportions of the ancestor and descendant populations. Apparently gradual changes in 'mean form' may be caused by natural selection operating on a continuous range of variation in populations living in environments lacking barriers to gene flow.

Macroevolution is concerned with evolution above the species level, the origins and extinctions of major groups and adaptive radiations. Microevolution and

Amplitude of second eigenfunction

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12.8

Amplitude of second eigenfunction

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Lohmann And Malmgren 1983

Fig. 2.1 Changes in morphology and habitat during the evolution of the planktonic foraminifera Fohsella from the mid-Miocene. On the left, frequency histograms show the gradual (anagenetic) change in the morphology of the shell outline. On the right, stable oxygen isotope data from the same specimens show an abrupt appearance of a new thermocline-reproducing species (cladogenesis). The ancestor became extinct ~70 kyr after the appearance of the descendant species. Morphological data suggest that no more than one population was present at any one time. (Redrawn from Norris et al. 1996 with permission.)

Surface-reproducing species

Thermocline-reproducing species

Thermocline-reproducing species

Fig. 2.1 Changes in morphology and habitat during the evolution of the planktonic foraminifera Fohsella from the mid-Miocene. On the left, frequency histograms show the gradual (anagenetic) change in the morphology of the shell outline. On the right, stable oxygen isotope data from the same specimens show an abrupt appearance of a new thermocline-reproducing species (cladogenesis). The ancestor became extinct ~70 kyr after the appearance of the descendant species. Morphological data suggest that no more than one population was present at any one time. (Redrawn from Norris et al. 1996 with permission.)

macroevolution processes are decoupled (Stanley 1979). This is because the individual is the basic unit of selection in microevolution whilst selection between species may occur at higher levels, although the notion of competition and natural selection occurring between higher taxonomic categories is not unanimously accepted (see Kemp 1999). New structures, body plans and biochemical systems, and the characters of high taxonomic categories, appear suddenly in the fossil record, for example the appearance of calcification in the calcareous nannoplankton in the Early Mesozoic. The evolutionary mechanisms behind these changes are the least well understood of evolutionary phenomena. Explanations invoke mutation in regulatory genes, which encode for hormones and other rate-

effecting proteins and wholesale changes in chromosomal structure.

Mass extinctions are probably the most widely studied of the macroevolutionary patterns. These differ from 'background' extinction events in their speed (commonly <5 Myr) and intensity (where 20-50% of marine biodiversity may disappear in a single event). The Cretaceous-Tertiary boundary mass extinction provides the best-studied example of a mass extinction event. This been documented globally and has been attributed to a variety of terrestrial (including climate change) and extraterrestrial (meteorite impact) causes (see Hallam & Wignall 1997 for a review). A comprehensive review of the biological effects of the K-T mass extinction event is provided by MacLeod & Keller

(1996). Patterns of extinction in individual groups add little to the debate on the cause of the K-T mass extinction. For example, extinctions in planktonic foramin-ifera extend over an interval of 30 cm (<100,000 years) that spans the boundary and exhibit a preferential extinction of large ornate forms. Benthic foraminifera declined in diversity but were much less affected. Coc-colithophorids were once thought to become almost extinct at this boundary, however Cretaceous species found in the lower Tertiary are now considered to have survived the event (Perch-Nielsen et al. 1982). Dino-flagellates were evidently less affected by events at the boundary. Dinoflagellate cysts are extremely abundant in the boundary clay, indicating that environmental conditions were ideal for stimulating dinoflagellate blooms. Diversity and species turnover rates are also high across the boundary. Plants on the other hand show major changes, Wolfe & Upchurch (1986) noted the decline in pollen and a sharp peak in fern spores, suggesting the influence of wildfires, though increasing humidity could also have caused an increase in fern abundance.

Mechanisms of cladogenesis

Models of cladogenesis rely upon the genetic isolation of a population. Random mutations in these small populations (peripheral isolates) are then quickly spread and eventually lead to the development of a new species, a process known as allopatric speciation (Fig. 2.2). In the marine realm genetic isolation would at first sight seem less probable. However a number of ecological barriers are present in the oceans. For example, ocean frontal systems, such as the Tasman Front, a boundary between tropical and subtropical water masses, have been proposed as effective barriers to dispersal and may have been important in promoting allopatric speciation in globoconelid planktonic foraminifera during the Pliocene (Wei & Kennett 1988). Vicariant models of speciation similarly subdivide an original population into smaller units through the development of physical barriers such as land barriers, sea-level fall and the strengthening of water mass boundaries. Knowlton & Weight (1998) have documented many examples of vicariant speciation in the marine realm following the separation of the Atlantic and the Pacific oceans through circulation changes during the Pleistocene. Low sea levels during the Pleistocene have also been implicated in the speciation of copepods on either side of the Indonesian Seaway (Fleminger 1986). However, many planktonic fora-minifera species have the ability to cross such major barriers; Pullenatina obliquiloculata and other related species repeatedly reinvaded the tropical Atlantic from the Indo-Pacific during Pleistocene glacial cycles. Neither equatorial upwelling in the Atlantic nor the Isthmus of Panama were sufficient barriers to dispersal.

Many microfossil groups are planktonic and have high population sizes and high dispersal potential. These features would seem contrary to the conditions required for allopatric speciation. Species models that allow restricted genetic exchange may therefore be better explanations of speciation in these types of organisms.

Variation in morphology along geographical gradients (clines) can result in limited interaction between the ends of the cline and effective genetic isolation ('isolation-by-distance' or parapatric speciation). Clinal trends have been described in a wide range of marine planktonic organisms (van Soest 1975; Lohmann & Malmgren 1983; Lohmann 1992), though some believe these may represent geographical successions of distinct species (see below). Even the classical latitudinal morphological cline of Globorotalia truncatulinoides, originally described as continuous (Lohmann & Malmgren 1983) may contain distinct species (Healy-Williams et al. 1985; de Vargas et al. 2001).

Similarly 'isolation-by-ecology' appears common, and is particularly well documented for depth in fora-minifera. Many forams reproduce by sinking (Norris et al. 1996), during which they cross the large number of physical and chemical barriers in the ocean. It seems plausible that speciation could occur by changes in the depth of reproduction, though confirmatory evidence is still rather sparse. Norris et al. (1993, 1996) used stable oxygen isotopes to show that the evolution of Fohsella fohsi in the mid-Miocene involved a rapid shift in reproductive depth habitat (Fig. 2.1). Using similar methodology Pearson et al. (1997) calculated 1-2°C differences in the temperature at which calcification occurred in closely related species, relating this to differences in either season or depth of growth. As

Oceanographic front

Overlapping ranges

Tectonic barrier

Species 1

Peripheral Isolate

Oceanographic front

Overlapping ranges

Tectonic barrier

Species 1

Peripheral Isolate

(a) Allopatry

(b) Parapatry

(c) Vicariance

(a) Allopatry

(b) Parapatry

(c) Vicariance

(d) Depth parapatry

(Change in place of reproduction)

(e) Seasonal sympatry

(Change in timing of reproduction)

Fig. 2.2 Speciation models. (a) Allopatry, created by divergence on either side of a hydrographic boundary. (b,d) Parapatry in which species diverge along a gradual hydrographic gradient, for example a gradually changing thermocline depth (b) or depth (d). (c) Vicariance, occurs where a physical boundary creates isolation and the formation of a new species. (e) 'Seasonal sympatry' in which isolation is caused by a change in the timing of reproduction. In marine planktonic species complete genetic isolation as indicated in (a) and (c) is unlikely. (Redrawn after Norris 2000 with permission.)

the seasonal range in temperature of surface waters in the tropics and subtropics can be greater than this it is reasonable that divergence in these species could have occurred as the result of a shift in timing of reproduction and growth ('seasonal sympatry').

Theoretical and empirical studies (e.g. Howard & Berlocher 1998) have also indicated sympatric speciation may be more common in the marine realm than has been hitherto considered. Sympatry may have resulted from individuals evolving different strategies to avoid strong competition for a single food source (Dieckmann & Doebell 1999), or from disruptive selection which favours individuals with extreme characters, for example large and small predators at the behest of medium sized individuals (e.g. Kondrashov & Kondrashov 1999; Tregenza & Butlin 1999).

Biodiversity in the marine plankton

Briggs (1994) calculated there are approximately 12 million terrestrial multicellular species (approximately 10 million of which are insects!) but only 200,000 marine taxa. These are surprising numbers when models of ecosystem size, energy flow and environmental stability predict substantially higher numbers of marine to terrestrial taxa (Briggs 1994). Are the models or numbers incorrect?

Results of molecular phylogenetic analyses indicate there is a high cryptic biodiversity in the oceans. Numerous sibling species can be diagnosed using molecular sequence data but show few if any morphological differences (e.g. Bucklin 1986; Bucklin et al. 1996; Bucklin & Wiebe 1998), a feature that probably extends into the cyanobacteria (Moore et al. 1998) and bacterio-plankton (De Long et al. 1994). Cryptic speciation and high genetic diversity has also been documented for planktonic foraminifera (Huber et al. 1997; de Vargas & Pawlowski 1998; Darling et al. 1999; de Vargas et al. 1999) and, surprisingly, many morphologically similar taxa have ancient divergences. Distinguishing sibling species in the fossil record is extremely difficult and many previously defined ecological variants (ecophenotypes) may be distinct species; if this is the case then planktonic biodiversity has been grossly underestimated.

Reconstructing phylogeny

The higher classification (above species level) of a group of organisms should reflect their evolution. The taxonomic hierarchy is expressed as an upwardly inclusive nested heirarchy, similar species are grouped into genera, similar genera into families, families into orders, orders into classes and classes into phyla and where necessary subdivisions of these major categories, for example subfamily and superfamily, are also used. Higher taxonomic categories are distinguished by their suffix (i.e. -ae, -a, etc.) and many examples are included in subsequent chapters.

Defining higher taxonomic groupings is a largely subjective exercise. Until the 1970s classical taxon-omists used a combination of morphological (or phenetic) similarity and phylogenetic (evolutionary) resemblance, based on ill-defined notions of ancestor-descendant relationships. Stratigraphical succession of species and their geographical distribution played an important role in establishing phyloge-netic relationships. Since the 1970s an attempt has been made to reduce the subjectivity inherent in the classical method and two philosophical approaches have been followed. Phenetics (or numerical taxonomy) relies on scoring of characters. Cluster analysis and distance statistics can then be used on the resulting character matrix to quantify the similarities between taxa and groupings into higher taxonomic categories. Cladistics (or phylogenetic systematics), founded by W. Hennig (1966) has been much more widely applied to palaeontology though less so in micropalaeonto-logy. The reader is referred to Smith (1994) for a comprehensive explanation of the methodology. At the heart of cladistics is the concept that organisms contain a combination of 'primitive' (symplesiomor-phic) and evolutionary novelties (synapomorphic) or 'derived characters'. Closely related groups will share derived characters and these will distinguish them from other groups. For example, humans have a backbone, a primitive character of all vertebrates, and an opposable thumb, a derived character shared with our nearest relatives the great apes. A primitive character for all vertebrates, the backbone, is of course a derived character as compared to invertebrates. Synapomorphy and symplesiomorphy are therefore relative conditions of particular characters with reference to a particular phylogenetic reconstruction.

The results of a phylogenetic analysis are expressed in a cladogram, in which branching points are arranged in nested hierarchies. In the example in Fig. 2.3 C and D share a unique common ancestor, they are sister groups and share a synapomorphy not possessed by B. Thus B is the sister group of the combined grouping C + D and A is the sister group of B + C + D. If a large number of characters and taxa are being analysed the character matrix is routinely manipulated by computer programs such as paup (Phylogenetic Analysis Using Parsimony). This is a technique that makes the fewest assumptions (parsimony) to rank the set of observations and produce the cladogram. A cladogram

Cladogram Xyz
Fig. 2.3 A cladogram showing the phylogenetic relationship between A and D (see text for explanation).

is not an evolutionary tree but a hypothesis of relationships. Stratigraphical succession is explicitly ignored in the analysis. Once the cladogram has been produced stratigraphical succession can be used in the analysis of the cladogram (see Smith 1994) and to constrain the splitting of lineages in time. At this point the clado-gram becomes a phylogenetic tree.

Distinguishing shared primitive (sympleisiomor-phic) and shared derived (synapomorphic) characters is achieved by outgroup analysis. Here the ingroup, the group being studied, is compared to a closely related outgroup. In Fig. 2.3 B + C + D could be the ingroup and A the outgroup. Any character present in a variable state in the ingroup and found in the outgroup must be plesiomorphic (primitive). Apomor-phic characters are those only found in the ingroup.

Three types of cladistic groups have been defined: monophyletic groups contain the common ancestor and all of its subsequent descendants; paraphyletic groups are descended from a common ancestor (usually extinct) but do not include all the descendants; polyphyletic groups are the result of convergent evolution. In the latter, their representatives are descended from different ancestors and though looking superficially similar, there is no close phylogenetic relationship.

Subjectivity cannot be entirely removed from phy-logenetic reconstruction and higher taxonomic categories. In cladistics equally parsimonious cladograms can result from the analysis and choosing between these may become subjective. In numerical taxonomy the methods of measurement and the relative weighting given to characters are also subjective decisions. The possibility of morphological convergence during evolution is a problem for all taxonomic methods and ultimately molecular sequence data may be required to distinguish between polyphyletic and sibling species. Unfortunately such data are not available in extinct groups.

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  • serena
    What is gradualism Cryptic speciation in globorotaliid foraminifera?
    8 years ago

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