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- Life history strategies among Cupuladriids
- Classification of modes of propagation
Abstract: Cupuladriid cheilostome bryozoans can make new colonies both sexually and asexually. Sexual (aclonal) colonies are derived from larvae while asexual (clonal) colonies result from the fragmentation or division of larger colonies. A number of specialised morphologies exist which either enhance or discourage clonality, and cupuladriids preserve these in their skeletons, meaning that it is possible to count the abundances of individual modes of reproduction in fossil assemblages, and thus measure the mode and tempo of evolution of life histories using fossil colonies. In this paper we categorise, illustrate and describe the various clonal and aclonal methods of propagation in cupuladriids through the Cenozoic. Sexual reproduction is the only aclonal method of propagation, while four clonal methods are described comprising: (1) mechanical fragmentation, (2) autofragmentation, (3) colonial budding and (4) peripheral fragmentation. The processes involved in each are discussed and we explain how their prevalence can be measured in the fossil record using preservable morphologies. Compiling a record of the occurrence and distribution of the various modes of propagation through time and space we discover a general trend of evolution towards more complex modes in all three cupuladriid genera, but a geologically recent extinction of some modes of propagation that has left the present-day assemblage relatively depauperate. We see striking similarities in the general timing of expansion of modes of reproduction between the two most important genera, Cupuladria and Discoporella, although it is clear that Discoporella evolved a much wider range of special morphologies either to enhance or to discourage clonality than did Cupuladria.
One of the many advantages of a colonial over a solitary (unitary) lifestyle is the ease with which clonal (asexual) dispersal can take place (Hughes and Jackson 1985; Jackson and Coates 1986). Solitary organisms usually require complex processes to clone (including parthenogenesis), while the modular construction of colonies facilitates clonality because their modules (e.g. zooids, polyps) are often able to survive individually or in small groups. Thus, all that is required is for the colony to divide, either by itself or through breakage, and then regenerate from each separated part (ramet). The ability to clone provides a species with a distinct method of dispersal that avoids a number of risks associated with sexual reproduction (Jackson 1977), including increased size-dependent mortality and reliance upon gamete production. All major groups of extinct and extant colonial organisms have at some time employed clonal methods for dispersal, and clonal propagation has been important in the evolutionary success of many clades (Highsmith 1982; Jackson and Coates 1986; Urbanek and Uchmanski 1990), particularly for reef framework builders.
Measuring the relative proportion of clonal vs. aclonal individuals in a population of a colonial animal can be problematic. Molecular approaches, such as those employed by Foster et al. (2007), provide highly informative data but become extraordinarily laborious as the numbers of individuals incorporated increases. Normally, using morphology is no less challenging as the reproductive origin of individuals for the majority of colonial animals is irretrievable because the founding part of the colony is often not visible (Hughes and Jackson 1980, 1985; Hughes 1984). Because of this very fact, the fossil record has added little to our understanding of the evolutionary dynamics of clonal and aclonal propagation (but see Thomsen and Håkansson 1995; Cheetham et al. 2001; Håkansson and Thomsen 2001).
Cupuladriid bryozoans unambiguously preserve the reproductive origin in the calcified skeletons of both living and fossil colonies (O’Dea et al. 2004). Colonies from a sexually recruited larva show orderly radial budding from a central origin, while clonal colonies tend to have slightly asymmetrical forms and include the fragment from which they regenerated (Text-fig. 1). Cupuladriids have a rich Palaeogene and Neogene fossil record and are common in tropical seas today (Cook and Chimonides 1983); as such, cupuladriids are valuable tools for exploring the consequences of clonality through evolutionary time.
Figure TEXT-FIG. 1.. Aclonal colonies (top) of cupuladriids have an unmistakable radial budding pattern and produce ancestrular zooids that originate from the metamorphosis of a sexually produced larvae, while clonal colonies (bottom) have no ancestral region but possesses evidence of fragmentation or separation and the ensuing regenerative growth; × 7.
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Recent advances in the understanding of the life histories of living cupuladriids (Håkansson and Thomsen 2001; O’Dea 2006) have revealed that clonal propagation can occur in many different ways, each with their own morphological signature that is preserved in the fossil record. It is necessary to describe these various modes of propagation and their preservable morphological features before using cupuladriids as a model evolutionary system.
Accordingly, this paper reviews and clarifies the currently known modes of propagation in cupuladriids, introduces and describes previously undescribed modes of propagation, compiles and figures all known modes of propagation for future classification, and discusses their potential ecological and evolutionary significance. The paper focuses principally on the Neogene and Recent of the Caribbean and eastern tropical Pacific because this is currently the most intensively studied region and is potentially the most valuable for evolutionary studies because of the exhaustive record of Neogene cupuladriids that exists owing to the collections of the Panama Paleontology Project (PPP) (Collins and Coates 1999; Cheetham and Jackson 2000).
Life history strategies among Cupuladriids
- Top of page
- Life history strategies among Cupuladriids
- Classification of modes of propagation
The family Cupuladriidae comprises three genera, CupuladriaCanu and Bassler, 1919, Discoporella d’Orbigny, 1852 and ReussirellaBaluk and Radwanski, 1984; each of which adopts a semi-mobile, free-living life habit (Cook 1965; Baluk and Radwanski 1984; Cook and Chimonides 1994; Rosso 1996). Unlike most other bryozoans that live attached to rocks, shells or macroalgae, cupuladriids are unattached and rest on or within the sea-floor sediment. Colonies possess polymorphic zooids called vibracula with long setae that can be used to aid in the removal of sediment from the colony surface, movement up through sediment if buried, and even walking.
The oldest fossil record of the family is from the early part of the Palaeogene in Senegal (Gorodiski and Balavoine 1962). The group then seems to have spread into Asia in the Eocene, subsequently followed by a rapid widening of their range in the Miocene to Australia and the Americas (Lagaaij 1963; Rosso 1996). However, the evolutionary origins of the family remain enigmatic (Cook and Chimonides 1983), and an Asian origin of the family cannot be ruled out given the dearth of collections from the region. The distribution of both fossil and Recent species is tropical to subtropical and they are almost always associated with sandy or silty sea-floors, often in great abundance (Winston 1988; Rosso 1996).
Present-day tropical American cupuladriids exhibit a wide range of life history strategies. Some species propagate entirely clonally whereas others make all new colonies entirely aclonally. Many other species have a roughly equal mix of clonal and aclonal colonies, and are clearly able to interchange between the two modes from generation to generation (O’Dea et al. 2004). Although the mechanisms are not understood, there is a strong positive correlation between the prevalence of clonality and the levels of food available both among and within species (O’Dea et al. 2004; O’Dea 2006). It appears that higher food levels are more beneficial for clonal propagation because cloning requires ‘vegetative’ growth of the colony and growth rates increase with increasing food levels, and also because higher food levels may be necessary for the successful regeneration of a fragment.
Morphological features, such as the degree of calcification and shape of colonies, also correlate strongly with the prevalence of clonality (Håkansson and Thomsen 2001; O’Dea et al. 2004). Essentially, species that produce large, indeterminately growing colonies are lightly calcified, which helps promote fragmentation and, thus, their populations tend to be clonal. On the other hand, species that produce small, determinately growing colonies and are more heavily calcified tend to be aclonal as they are more resistant to fragmentation (Winston 1988; Håkansson and Thomsen 2001; O’Dea et al. 2004). If clonal propagation of new colonies is the result of external forces causing the breakage of colonies, cupuladriid morphology can either promote or inhibit fragmentation. As such, strength and size of colonies may, therefore, be adaptive features that control reproductive life history strategy. The preservable features of fossils can thus be used to explore detailed evolutionary changes in life histories.
When clonal propagation in cupuladriids was first studied, the fragmentation of colonies was attributed either to high energy currents or waves (Dartevelle 1935), or to the breakage of colonies during grazing by other animals (Greeley 1967). Combined, these modes of cloning are termed mechanical fragmentation because they require external forces to break the colony (O’Dea 2006). Some cupuladriids, however, do not rely on chance to fragment and clone, but are able to control when, where and how fragmentation takes place using a variety of special morphologies. Colonies of Cupuladria exfragminis from the Pacific coast of Panama are able to autofragment, i.e. separate their colonies into parts without the need for external force (O’Dea 2006), and appear to do so in synchrony when conditions are favourable. Fossil colonies of the Miocene Ruessirella haidingeri were probably able to detach colony buds by removal of an uncalcified connection between bud and parent colony (Håkansson and Thomsen 2001).
Basic discrimination between clonal and aclonal colonies is straightforward based on simple morphological differences (Cook 1965), which are normally so striking that colonies can be distinguished with the naked eye despite their small size (Text-fig. 1). Discriminating the variety of different modes of clonal propagation, however, requires more attention to detail. Although the resulting colonies from each clonal mode are somewhat morphologically similar, and discriminating between some of the modes is often difficult, it is still possible to categorise the majority of clonal colonies using detailed features that are preserved in the skeleton.
The following section describes five modes of propagation in cupuladriids. For each mode we (1) illustrate the life cycle, (2) figure a range of examples, (3) describe the process of propagation and (4) list the preservable (hard skeleton) morphologies that can be used to distinguish them in fossil material.
Acknowledgements. We thank Tania Romero, Anthony Coates, Rachel Collin, Gabriel Jacome, Travis Smith, Sebastian Castillo, Eric Brown and the crew of the R/V Urraca for helping to make collections of fossil and Recent cupuladriids. Andrei Ostrovsky helped with Text-figure 2 and Carlos De Gracia and John Christy with Text-figure 4. Discussions with Eckart Håkansson, Drude Molbo, Beth Okamura, Holger Anlauf, Steve Vollmer and Amalia Herrera helped improve many of the ideas presented here. The Panamanian Recursos Minerales kindly gave permission to collect fossil material. Funding was provided by the National Science Foundation (EAR03-45471), the Smithsonian Marine Science Network, the Smithsonian Tropical Research Institute, and the National Geographic Society.