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Asexual Reproduction of Marine Invertebrate Embryos and Larvae W&M ScholarWorks Arts & Sciences Book Chapters Arts and Sciences 1-2018 Asexual Reproduction of Marine Invertebrate Embryos and Larvae Jonathan D. Allen College of William and Mary, [email protected] Adam M. Reitzel William Jaeckel Follow this and additional works at: https://scholarworks.wm.edu/asbookchapters Part of the Marine Biology Commons Recommended Citation Allen, J. D., Reitzel, A. M., and Jaeckle, W., Asexual reproduction of marine invertebrate embryos and larvae. In. Evolutionary Ecology of Marine Invertebrate Larvae. (2018). Edited by Tyler J. Carrier, Adam M. Reitzel, and Andreas Heyland: Oxford University Press. This Book Chapter is brought to you for free and open access by the Arts and Sciences at W&M ScholarWorks. It has been accepted for inclusion in Arts & Sciences Book Chapters by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. Chapter 5 Asexual Reproduction of Marine Invertebrate Embryos and Larvae Jonathan D. Allen, Adam M. Reitzel, and William Jaeckle 5.1 Introduction addressed with respect to such aspects of sexual re- production as facultative progenesis, where larval The life histories of marine invertebrates are incred- stages develop gametes (Poulin, 2001), and poecil- ibly diverse and provide a wealth of opportunities ogony, where one individual or species exhibits dif- to develop and test hypotheses about how and why ferent reproductive modes (Krug, 1998). One area of modes of reproduction, development, and behav- life history plasticity that is far more common, but ior evolve within and among lineages. With respect has received less attention, is asexual reproduction. to the evolution of reproductive and developmen- Asexual reproduction during development oc- tal mode, phylogenetic, adaptive, and functional curs in most marine phyla (reviewed by Alvarado, hypotheses presented over the past century have 2000; Blackstone and Jasker, 2003) and may occur predominantly focused on the evolution of repro- at multiple stages during the indirect development ductive traits (e.g., free spawning, brooding, en- of some species. Despite, or perhaps because of, its capsulation; Rouse and Fitzhugh, 1994), nutritional broad distribution among phyla, diverse explana- mode of larvae (e.g., planktotrophy and lecithotro- tions for the adaptive value or evolutionary sig- phy; Strathmann, 1985; Hart et al., 1997), and devel- nificance of asexual reproduction as a life history opmental form (e.g., larval morphology; Jeffery and strategy have been offered. Adaptive explanations Swalla, 1992; direct and indirect development; Wray, include the following: as a method to weather 1995; McEdward and Janies, 1997). Frequently, but harsh environments (e.g., gemmules in sponges, not exclusively, these hypotheses have been tied to statoblasts in bryozoans); as a short-term solution changes in per-offspring investment (Emlet et al., for escaping mutation load (Hurst and Peck, 1996); 1987; Sinervo and McEdward, 1988; Emlet and as a means to colonize and/or adapt to chang- Hoegh-Guldberg, 1997), and influential models of ing or new habitats (Maynard Smith, 1971); or as per-offspring investment often serve as a frame- a means to persist at low population sizes (Gerber work for studies of the evolution of developmen- and Kokko, 2016). Several authors have addressed tal modes (Vance, 1973; Christiansen and Fenchel, adult asexual propagation and regeneration across 1979; Levita n, 2000). Phylogenetic assessment of the animal kingdom (e.g., Ferretti and Geraudie the evolution of character states within lineages has 2001), but asexual propagation is also employed by revealed frequent shifts among life histories traits pre-adult stages. In this chapter we aim to synthe- (McHugh and Rouse, 1998, and references therein). size the literature describing asexual reproduction In addition to these macroevolutionary changes by embryonic and larval stages of marine inver- among species, the life history exhibited by indi- tebrates, with a particular focus on echinoderms, viduals may change in response to one or more where the ecological and evolutionary costs and environmental features (life history plasticity). Plas- benefits of diverse modes of clonal replication have ticity in the evolution of life histories has also been been most studied. We conclude with a list of open Allen, J. D., Reitzel, A. M., and Jaeckle, W., Asexual reproduction of marine invertebrate embryos and larvae. In. Evolutionary Ecology of Marine Invertebrate Larvae. Edited by Tyler J. Carrier, Adam M. Reitzel, and Andreas Heyland: Oxford University Press (2018). © Oxford University Press. DOI: 10.1093/oso/9780198786962.003.0005 68 EVOLUTIONARY ECOLOGY OF MARINE INVERTEBRATE LARVAE questions that may provide fruitful future research may also undergo facultative asexual propagation avenues to better understand this understudied life to yield many hundreds of embryos that complete history trait of marine invertebrates. development and that are released as lecithotrophic larvae. Polyembryony has been described for one 5.2 Types of Asexual Reproduction species of cnidarian, the coral Acropora millepora, of and by Embryos and Larvae where environmental turbulence fragments early embryos and the isolated blastomeres can develop The general life history of a marine invertebrate into complete larvae (Heyward and Negri, 2012). has two potential stages where asexual propaga- Among echinoderms, polyembryony has been ob- tion could occur after fertilization, but prior to served in five species from the class Echinoidea: the the development of the adult stage: the develop- sea urchins Prionocidaris baculosa (Mortensen, 1938), ing embryo and, when present, the larva. Asexual Eucidaris tribuloides, Lytechinus variegatus, and Stron- reproduction in various marine invertebrates, as gylocentrotus droebachiensis, and the sand dollar Echi- well as throughout all animal phyla, also occurs narachnius parma (Allen et al., 2015). The incidence of by an elimination of meiosis during reproduction polyembryony in these species is highly variable and (e.g., parthenogenesis, apomixis, automixis; Judson significantly impacted by changes in environmental and Normark, 1996) and during the juvenile/adult conditions (e.g., salinity, discussed later). Finally, a stage (Blackstone and Jasker, 2003). species of ectoparasitic flatworm (phylum Platyhel- minthes), Gyrodactylus elegans, also exhibits polyem- bryony but through a different mechanism involving 5.2.1 Embryo unequal cleavage, instead of embryo fragmentation. Asexual propagation at the embryo stage is referred For this species, a single fertilized egg undergoes to as polyembryony. Polyembryony is defined as unequal cleavage that produces a second embryo the splitting of one sexually produced embryo into within the initial embryo, a third embryo within the many independent individuals. Approximately 20 second, and a fourth embryo within the third (Kath- years ago, Craig et al. (1997) reviewed the occur- eriner, 1904). rence of polyembryony in animals. They included both fragmentation of embryonic stages and larval 5.2.2 Larva budding within the term polyembryony, whereas here we will limit our definition of polyembryony to Asexual propagation at the larval stage has been re- asexual propagation prior to the formation of a de- ported in at least four phyla: Arthropoda, Cnidaria, finitive larva. Embryos and larvae commonly have Neodermata (within the traditional phylum Platy- different levels or degrees of tissue and structural helminthes), and Echinodermata (addressed in a organization, which allow for different mechanisms separate section later). For those species where it of asexual reproduction. For some terrestrial species has been described, asexual propagation occurs (e.g., nine-banded armadillos and various species by budding, although the method of budding can of parasitoid wasps), polyembryony is an obligate be quite variable. Within the phylum Arthropoda, part of the life history where a single fertilized oo- the parasitic rhizocephalan barnacles display a bi- cyte fragments to result in more than one develop- zarre method of larval budding, where they use ing embryo. Polyembryony has also been reported totipotent cells for host invasion (Glenner and in a handful of species from the Bryozoa, Cnidaria, Høeg, 1995). The cyprid larva settles on a decapod Echinodermata, and Platyhelminthes. Some spe- host and transforms into a kentrogon, which then cies of cyclostome bryozoans (e.g., Crisia denticulata; injects a number of de-differentiated cells into the Hughes et al., 2005) exhibit polyembryony via frag- host. Each cell forms a vermiform stage that splits mentation of the cleaving embryo. Adults produce into individual cells that will form independ- one or two primary embryos in the gonozooid that in ent adults in different parts of the host. A similar turn divide to produce up to 100 secondary embryos “infective” single-cell stage may occur via amoe- (reviewed in Reed, 1991). These secondary embryos boid cells in narcomedusozoans (Russell, 1953), ASEXUAL REPRODUCTION OF MARINE INVERTEBRATE EMBRYOS AND LARVAE 69 although the specific details are limited. For other infrequently observed and there is one larval form species of narcomedusan hydrozoans (Osborn, (tentatively assigned to the taxonomic order Paxil- 2000), scyphozoan s (Berrill, 1949), one species of sea losida, family Astropectinidae) that asexually re- anemone (Edwardsiella lineata; Reitzel et al., 2009), produces by autotomy
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