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Asexual of Marine and Larvae

Jonathan D. Allen College of William and Mary, [email protected]

Adam M. Reitzel

William Jaeckel

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Recommended Citation Allen, J. D., Reitzel, A. M., and Jaeckle, W., of marine invertebrate embryos and larvae. In. Evolutionary of Marine Invertebrate Larvae. (2018). Edited by Tyler J. Carrier, Adam M. Reitzel, and Andreas Heyland: Oxford University Press.

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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 histories of marine are incred- stages develop (Poulin, 2001), and poecil- ibly diverse and provide a wealth of opportunities ogony, where one individual or 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 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 , not exclusively, these hypotheses have been tied to statoblasts in bryozoans); as a short-term solution changes in per- investment (Emlet et al., for escaping 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 (Maynard Smith, 1971); or as per-offspring investment often serve as a frame- a means to persist at low sizes (Gerber work for studies of the evolution of developmen- and Kokko, 2016). Several authors have addressed tal modes (Vance, 1973; Christiansen and Fenchel, asexual propagation and across 1979; Levitan,­ 2000). Phylogenetic assessment of the (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 , 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 . development and that are released as lecithotrophic larvae. has been described for one 5.2 Types of Asexual Reproduction species of cnidarian, the 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- urchins Prionocidaris baculosa (Mortensen, 1938), ing and, when present, the . Asexual Eucidaris tribuloides, Lytechinus variegatus, and Stron- reproduction in various marine invertebrates, as gylocentrotus droebachiensis, and the Echi- well as throughout all animal phyla, also occurs narachnius parma (Allen et al., 2015). The incidence of by an elimination of during reproduction polyembryony in these species is highly variable and (e.g., , , automixis; Judson significantly impacted by changes in environmental and Normark, 1996) and during the /adult conditions (e.g., salinity, discussed later). Finally, a stage (Blackstone and Jasker, 2003). species of ectoparasitic (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 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 . They included both fragmentation of embryonic stages and larval 5.2.2 Larva 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, , finitive larva. Embryos and larvae commonly have (within the traditional phylum Platy- different levels or degrees of 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 ), polyembryony is an obligate be quite variable. Within the phylum Arthropoda, part of the life history where a single fertilized oo- the parasitic rhizocephalan 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 , 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 forms a vermiform stage that splits mentation of the cleaving embryo. 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 Paxil- 2000), scyphozoan­s (Berrill, 1949), one species of sea losida, family Astropectinidae) that asexually re- anemone (Edwardsiella lineata; Reitzel et al., 2009), produces by autotomy of the preoral lobe (Jaeckle,­ and trematodes and cestodes (Katheriner, 1904; 1994). Poulin, 2007), a larva asexually propagates by - by ophiuroid larvae was originally sug- ding from the existing larval tissue. gested by Mortensen (1921) and described by Balser (1998) involving similar morphological changes to 5.3 Asexual Reproduction by Feeding those observed in asteroids, but the clone is formed after the separation of the larval body from the fully Larvae of Echinoderms formed juvenile. The remnants of the “primary” 5.3.1 Class-level Distribution of Larval Cloning larva migrate to the vertex of the posterolateral arms and reiterate gastrulation (by invagination) in Echinoderms and form the digestive system of the secondary Asexual propagation by larvae has been most larva. Balser (1998) reported that from a single thoroughly described for planktotrophic larvae fertilized egg of Ophiopholis aculeata two juveniles of echinoderms. A review by Mladenov (1996) could be formed and that the development of second summarized the occurrence of asexual reproduc- clonal generation for one individual was initiated. tion in classes and life history stages, Among asteroids, a cloning sequence similar to where 1.3% of species undergo asexual reproduc- that exhibited by ophioplutei is hypothetically pos- tion as adults (0% of crinoids and echinoids, up sible. Cloning by larvae could occur after a larva to 2.2% of ophiuroids). Asexual reproduction by and the fully formed juvenile separate as the larval feeding larvae of echinoderms is known from four remnant may reenter the water column (e.g., of five taxonomic classes (Asteroidea, Echinoidea, sarsi). Although the digestive system of the persist- ­Holothuroidea, and Ophiuroidea), and is not ing larval body contains only short esophageal and known for larvae from the Crinoidea. Larval clon- intestinal segments, these individuals can survive ing is more broadly distributed among echinoderm for some period of time (Tattersall and Sheppard, classes than adult asexual reproduction despite the 1934). However, in culture they appear to be inca- many fewer larval forms that have been studied, pable of feeding on particulate foods and “as far some exclusively from field samples. as Luidia sarsi is concerned, regeneration followed Of all reports, evidence of cloning by larvae in the by a second most probably never field is known only for some members of the Aster- occur­s” (Wilson, 1978, p. 475). oidea and Ophiuroidea (Bosch et al., 1989; Bosch, 1992; Rao et al., 1993; Jaeckle, 1994; Balser, 1998; 5.4 Modes of Asexual Reproduction Knott et al., 2003; Galac et al., 2016). In the subtrop- ical-tropical western Atlantic Ocean, asteroid larvae in Echinoderms showing evidence of current and past asexual re- 5.4.1 asexual Reproduction by Budding production by paratomy are seasonally abundant (Jaeckle, 1994; Knott et al., 2003). Rao et al. (1993) Larval budding has been reported for members of the also reported cloning larvae from the Bay of Ben- echinoderm classes Asteroidea (Jaeckle, 1994; Vick- gal (northeast Indian Ocean), and there is an image ery and McClintock, 2000), Holothuroidea (Eaves of a cloning bipinnaria larva collected from waters and Palmer, 2003), and Echinoidea (Vaughn and surrounding the Great Barrier Reef (Image Quest Strathmann, 2008; Vaughn, 2009; 2010; McDonald­ Marine, personal communication). Two other forms and Vaughn, 2010). The details of this form of asex- of asexual reproduction are exhibited by field- ual reproduction among groups are not well de- collected asteroid larvae from the tropical west- scribed and the developmental sequence of events is, ern Atlantic Ocean: the release of the tips of larval at best, superficially known. For asteroid larvae, the arms (budding) by newly collected larvae has been released apices of the larval arms appear to reiterate 70 Evolutionary Ecology of Marine Invertebrate Larvae the sequence of development from a fertilized egg. of the parent arm corresponds to the posterior side of Gastrulation by the blastula-stage secondary em- the offspring. How this axial inversion or any other bryos reportedly occurs through unipolar invagina- attribute of asexual reproduction is genetically speci- tion and the digestive system of the clone is derived fied or regulated has not been identified. from the ectoderm of the parent larva (Jaeckle, 1994). Transformation of the posterolateral arms into Although Jaeckle (1994) hypothesized that coelomo- new (secondary) individuals is morphologically genesis in these embryos occurs through schizocoely, signaled by the dissipation of the ciliary band that there are no new data that support this proposal. runs along the lateral sides of the posterolateral arm and the transformation of a simple epithelium into a stratified epithelium (Bosch et al., 1989). All 5.4.2 asexual Reproduction by Paratomy known forms of cloning exhibited by asteroid lar- Paratomous asexual reproduction by asteroid larvae vae involve an apparent re-differentiation of cell (Figure 5.1) is known from individuals collected in fates. During the paratomous transformation, the samples taken throughout the subtropical- presumptive ectoderm of the parent larva forms a tropical western Atlantic Ocean. To our knowledge, new “secondary archenteron,” which forms the di- in all examined clones formed by paratomy of the gestive system of the clone. posterolateral arms, the anterior-posterior axis of the The archenteron develops along the length of the developing clone is reversed to the anterior–posterior transforming arm (Bosch et al., 1989; Figure 5.2). axis of the parent arm; the proximal (anterior) portion


Cb M


S uM


Figure 5.1 Scanning electron micrograph (ventral view) of a field- collected early brachiolaria larva showing an unmodified posterolateral arm (uM, left side) and a clonal arm (cA, right side) where the Figure 5.2 light micrograph of a field-collected sea star larva with a posterolateral arm is transforming into a new “secondary” larva gastrula-stage secondary larva (SL) forming from the posterolateral arm. through the process of paratomy. Symbols: Cb = ciliary band, M = Symbols: A = archenteron of clone, E = esophagus of the primary larva, mouth. Scale bar = 200 μm. PL = primary larva, S = stomach of the primary larva. Scale bar = 200 μm. Asexual Reproduction of Marine Invertebrate Embryos and Larvae 71

However, it is unclear if the archenteron invaginates bipinnaria larva (Figure 5.4). Fully formed sec- as a longitudinal furrow that closes along its length ondary bipinnariae may ingest particles prior to to leave a circular posterior opening or if it forms separation from the parent larva. The only known from a single invagination that extends distally observation of the separation of the clone from the within the blastocoel of the transforming arm. After parent larva (of ) occurred as the the archenteron achieves its full length, the tubular clone rotated about the long axis of the transform- gut differentiates to become the esophagus, stomach, ing arm of the parent arm. This rotation tightened and intestine, and the mouth is established as a new the stricture between the parent and clone and re- opening on the distal side of the transforming arm. sulted in a breakage of the epithelial connection. formation during the development of the secondary (clonal) larva remains incompletely 5.4.3 asexual Reproduction by Autotomy described, but examination of physical and optical sections of cloning larvae indicates that secondary Mortensen (1898) illustrated a larva (“Auricularia coelomogenesis occurs by enterocoely (Figure 5.3). paradoxa”) collected from the tropical western At- Ultimately, a single presumptive coelom may lie lantic Ocean (0° 24’ N; 46° 40’ W) that resembles an lateral to the developing archenteron and extend asteroid larva with long posterolateral arms minus beyond the archenteron in the distal side of the the preoral lobe. He described this larva by writing, transforming larval arm. “The opening of the mouth seems to lie very close Clonally produced individuals may separate to the anterior end, but everything which should from the parent as an early stage or fully formed be above the anterior transverse margin is want- ing.” Whether this individual was an auricularia larva (Holothuroidea) that was damaged during

S-p PL I-p LS Cb


A A SL ? S


Figure 5.3 combined optical sections (N=3) of a ventral view of a primary larva (PL) with an attached secondary larva (SL) forming through Figure 5.4 combined optical sections (N=3) of a dorsal view of an the process of paratomy. The secondary archenteron (A) is continuous independent secondary larva formed by the process of paratomy. The with a blastopore (B) and a thin-walled cavity whose developmental left axohydrocoel (A) extends a pore canal that fuses with the outer fate is unresolved. Symbols: I-p = intestine of primary larva, LS = left epithelium (not shown), but there is no evidence of a right axohydrocoel. somatocoel of the primary larva, S-p = stomach of primary larva. The Symbols: Cb = ciliary band, E = esophagus, S = stomach. The specimen specimen was stained with Nile Red and examined using a Leica model was stained with Nile Red and examined using a Leica model TCS SP2 TCS SP2 scanning laser confocal microscope. Scale bar = 150 μm. scanning laser confocal microscope. Scale bar = 100 μm. 72 Evolutionary Ecology of Marine Invertebrate Larvae collection or an asteroid larva that had previously 5.5 Induction of Asexual Reproduction autotomized its preoral lobe is not known. Nearly 100 years later, Jaeckle (1994) described larvae col- Little is known about the factors that induce asex- lected from the subtropical western Atlantic Ocean ual reproduction in , but induction of poly- with a common phenotype—but different from the embryony and larval cloning have been achieved larva described by Mortensen—that reproduced by using a number of different cues in laboratory autotomy of the preoral lobe. Autotomization of settings. Understanding the forces responsible for the preoral lobe was then reported for cultured lar- inducing asexual reproduction, especially if they vae of several forcipulatid asteroids: Pisaster ochra- are rather common, may help us understand the ceus (Vickery and McClintock, 2000), Distolasterias frequency with which it occurs in nature. Studies nipon (Kitazawa and Komatsu 2001), and Asterias to date suggest both abiotic and biotic factors can forbesi (Blackburn and Allen, 2013, Figure 5.5). Au- result in larval cloning in different species. totomy by cultured pluteus larvae of the sand dol- lar Dendraster excentricus (order Clypeasteroida) 5.5.1 Abiotic was seen after larvae were exposed to mucus (Vaughn and Strathmann, 2008; Vaughn 2009; 2010) Abiotic cues of asexual reproduction include or acute increases in food abundance (MacDonald changes in environmental parameters, including and Vaughn, 2010). Despite multiple observations pH, salinity, temperature, and even the turbulence of this form of cloning, the mechanism of asexual of the water. Few studies have investigated the reproduction by autotomy is not known. degree to which these parameters (many of which Examination of the “new” bipinnaria larvae are projected to covary in models of future climate formed by autotomy of the preoral lobe of the change) may interact with one another to induce parent larva reveals apparent differences in the asexual reproduction. Independently, each condi- coelomic cavities. Examination of these small bi- tion has been demonstrated to play at least some pinnariae revealed a precocious development of role in inducing asexual reproduction and thus all the coelomic system, compared to a larva of similar are of great interest to both larval and ma- size formed from a fertilized egg. In one individual rine ecologists concerned about how recruitment at the time of collection, there was no evidence of a patterns vary in space and time. pore canal extending from the left axocoelic coelom There is recent interest in how ocean acidifica- or a dorsal pore (“hydropore”). tion will affect the small, often partially calcified

Day 7 Day 8 Day 9 Day 10 Day 11 Day 12 Day 19

Figure 5.5 Development/regeneration of the anterior portion of a bisected larva over 12 days. The preoral lobe was first observed floating in culture on Day 7. Arrowhead indicates larval mouth. Arrow indicates the reappearance of coelomic cavities. The dark coloration of the stomach on Day 19 indicates the presence of algal food following resumption of larval feeding. All images are at the same scale. Scale bar = 100 µm. All photos courtesy of Holly Blackburn. Asexual Reproduction of Marine Invertebrate Embryos and Larvae 73 developing stages of marine invertebrates (re- Mortensen (1938) suggested that polyembryony viewed by Byrne, 2011), but relatively little is known may occur as part of the normal developmental about the effect that acidification might have on the pathway in another cidaroid, Prionocidaris baculosa, propensity of embryos or larvae to clone. Chan et al. but provided no information on the environmen-

(2013) demonstrated that pCO2 levels predicted for tal conditions (temperature, salinity, etc.) at which 2100 and 2300 induced high frequencies (>50%) of embryos were raised. Interestingly, embryos of two budding for early larval stages of the purple sea ur- species of regular urchins (Strongylocentrotus droe- chin Strongylocentrotus purpuratus. However, none bachiensis and Lytechinus variegatus) have also been of the resultant survived for more than two tested for similar responses to salinity, but very days, calling into question the viability of asexually rarely exhibited polyembryony. produced and also raising the possibil- Environmental induction of polyembryony in ir- ity that methods for rearing buds may differ from regular echinoids but not in regular echinoids is con- those sufficient to culture primary embryos and lar- sistent with chemical induction of polyembryony vae. Low pH has also been reported to increase the as reported in a series of papers by Mazia and Vac- frequency of conjoined in larvae of the gastro- quier (Mazia, 1958; Vacquier and Mazia, 1968a; b). pod Crepidula fornicata (Eyster, 1995), but there is as Vacquier and Mazia (1968b) showed that the close yet little evidence that this occurs in nature or that association of blastomeres with the hyaline layer in unjoined twins are ever produced. regular echinoids kept cells pressed together even Temperature has also been shown to affect the when cell-cell adhesion was disrupted by applica- frequency of larval cloning in echinoderm larvae. In tion of dithiothreitol (DTT). In contrast, applica- asteroids, Vickery and McClintock (2000) reported tion of DTT to Dendraster excentricus embryos with that temperature exerted a strong effect on the like- a looser association with the hyaline layer resulted lihood of larval cloning in the bipinnariae of the sea in dissociation of cells from one another and ulti- star Pisaster ochraceus. At low temperatures (7–10 ºC) mately polyembryony. Since the presence of Ca2+ no larval cloning was observed, but at moderately ions is also required for normal interactions be- increased temperatures (12–15 ºC) cloning was ob- tween blastomeres (Vacquier and Mazia, 1968a; b), served in about 6% of larvae in culture. At more ex- it has been proposed that environmental induction treme levels of temperature (17–20 ºC) no cloning of polyembryony at low salinities may result from was observed, but this result may have been con- lower concentrations of Ca2 + in low-salinity seawa- founded with high levels of mortality among pri- ter (Allen et al., 2015), but this has yet to be formally mary larvae (Vickery and McClintock, 2000). tested. Regardless, the diversity of responses of Similarly, few studies have assessed the role of regular and irregular echinoids to similar environ- salinity as a factor that induces asexual reproduc- mental conditions suggests these lineages may be tion by echinoderm embryos. In 2015, Allen et al. promising models for future comparative studies of described the role of salinity as a cue inducing the mechanisms of asexual propagation of embryos. polyembryony in early embryos of two sea urchins, The combination of multiple stressors, either the cidaroid Eucidaris tribuloides and the echinoid taken from the previous list or unique ones not Echinarachnius parma. Reduced salinity resulted in yet considered, may be a fruitful area for future re- higher frequencies of polyembryony in both spe- search on the induction of asexual reproduction in cies, but also interacted significantly with increas- embryos and larvae. ing temperature to yield even higher frequencies of polyembryony. Similar results have been found 5.5.2 Biotic in a third echinoid species, the sand dollar Den- draster excentricus (Abdel Raheem and Allen, un- In addition to the abiotic stimuli described earlier, published data). The interaction between salinity there is increasing evidence that asexual reproduc- and temperature suggests that multiple factors may tion may also be induced by interactions between act in synergistic ways to influence frequencies of larvae and other in their environ- asexual reproduction (see later). Prior to this work, ment. Biotic stimuli suggested to induce asexual 74 Evolutionary Ecology of Marine Invertebrate Larvae reproduction include the amount of phytoplankton clones in response to fish mucus is highly variable in culture (Vickery and McClintock, 2000; Eaves and and appears to be influenced by genetic (maternal) Palmer, 2003), a sudden change in food abundance background (Vaughn, 2009). The reduced size of (McDonald and Vaughn, 2010), and the presence of larval clones relative to primary larvae has been chemical cues from a possible predator (Vaughn and suggested to be an adaptive response (Vaughn and Strathmann, 2008; Vaughn, 2009; 2010). The ability Strathmann, 2008; see further discussion later) to of larval stages to perceive and respond to biologi- visual predators that are known to be size-specifi­c cally produced chemical cues in their environment in their feeding on larval echinoids, preferring is well known, and can be manifested in a number of larger larvae to smaller ones (Allen, 2008; Vaughn, ways, including plasticity in arm length in response 2010). However, as with phytoplankton cues, the to phytoplankton food (e.g., Hart and Strathmann, prevalence of predator-induced cloning in nature is 1994; Miner, 2005), plasticity in shell morphology unknown and the mucus inducer of larval cloning in response to predators (Vaughn, 2007), delays in is isolated from a benthic fish (the dover sole, Micro- hatching time in response to predators (Miner et al., stomus pacificus) that feeds preferentially on benthic 2010), and plasticity in settlement time in response and ophiuroids as an adult (Gabriel to prey (Hadfield, 1977). Thus, it may not be sur- and Pearcy, 1981), although the lengthy pelagic prising that to the degree planktonic larvae are able period of its larvae may provide an opportunity to reproduce asexually, they do so in response to for planktivory on echinoids (Pearcy et al., 1977), biological cues in their environment. However, the though that has yet to be demonstrated. frequency of biologically induced cloning events in nature is unknown. Only in a handful of controlled laboratory studies do we have any evidence for bio- 5.6 Other Taxa logical induction of asexual reproduction. To date, only one study has examined the role of The most detailed examples of biotic stimuli in- environmental turbulence in asexual reproduc- ducing asexual reproduction come from studies of tion, occurring in the scleractinian coral Acropora the effects of larval food supply (i.e., phytoplankton millepora (Heyward and Negri, 2012). Cloned coral abundance) on clone production in echinoderms. embryos resulting from turbulence-induced blasto- In the ochre sea star, Pisaster ochraceus, Vickery mere separations at the two-, four-, and eight-cell and McClintock (2000) showed that cloning rates stages were able to successfully complete develop- were highest when phytoplankton food was most ment in the lab, albeit at smaller sizes. For embryos abundant in culture and that a mixed diet (multi- of A. millepora the levels of turbulence sufficient to ple species of phytoplankton) yielded higher rates induce cloning in the laboratory are equivalent to of cloning than did a single-species diet. Similarly, or less than those found in nature during the major- phytoplankton abundance is also a cue for cloning ity (52%) of spawning events on the Great Barrier in the pluteus larvae of the sand dollar, Dendraster Reef. It is therefore likely that natural turbulence excentricus (McDonald and Vaughn, 2010). In the generates cloned coral embryos, although the fate case of D. excentricus, however, it is not the level of these embryos and the potential adaptive value of phytoplankton abundance that induces cloning, of this response remains unknown. but rather a sudden shift in phytoplankton abun- dance (from low to high) that correlates with high frequencies (50–100% of larvae) of clone production 5.7 Is Larval Cloning Adaptive? (McDonald and Vaughn, 2010). Perhaps the most surprising example of biologi- As noted earlier, it is tempting to view asexual re- cal stimuli inducing clone production also comes production by embryos and larvae through the from D. excentricus, where pluteus larvae can be lens of , but the adaptive value of poorly induced to produce clones via budding after ex- understood phenotypes is difficult to demonstrate. posure to mucus cues from planktivorous fish The hypothesized benefits of asexual reproduc- (Vaughn and Strathmann, 2008). The production of tion by embryos and larvae are intuitive, related Asexual Reproduction of Marine Invertebrate Embryos and Larvae 75 to increasing the number of copies. They both lists of “consequences” are plausible, but re- could contribute to reproductive success in one or main largely untested. The net effect of cloning is more ways. Cloning: realized as the sum of these positive and negative consequences, and there is no a priori reason to ex- 1. increases without an apparent pect that the result of this summation is constant increase in allocation to reproduction; from year to year. 2. may increase in the likelihood that a member of a To our knowledge, there is only one formal at- genet survives; tempt to model the consequences of larval cloning. 3. may increase the probability that a member of Rogers-Bennett and Rogers (2008) evaluated the a genet will locate a suitable settlement site by influence of an unspecified form of larval cloning sampling a greater geographic area; on dispersal distance. Their simulations predicted 4. may reduce the genet’s susceptibility to loss (i.e., (1) that cloning increases the dispersal potential ) by increasing number; and of a cohort of larvae, and (2) that the age of par- 5. may reduce the genet’s susceptibility to loss ent larvae when asexually produced offspring are (i.e., predation) by decreasing propagule size released was positively related to the dispersal po- (Vaughn, 2010). tential of the cohort. Their model, however, did not Nevertheless, the formation of each new individual incorporate any estimates of the cost(s) of asexual (the clone) is a result of the loss of cell(s) from the reproduction to the parent larva or to the subse- “parent” embryo or larva, and this reduction in bio- quent juvenile. mass may negatively influence the larva, the result- Although the costs and benefits that may select ing juvenile, or both. The impact of this tissue loss for evolution of larval cloning in marine inverte- on the survivorship of the parent is unknown, but brates remain understudied in free-living marine it seems reasonable to hypothesize that the cost of species, asexual reproduction of developmental asexual reproduction to the parent embryo or larva stages in parasitic species are better characterized. could include: Endoparasitic larval stages of digeneans, cestodes, and other parasitic Platyhelminthes (Neodermata) 1. a decrease in larval feeding rate; commonly exhibit asexual propagation in inter- 2. a decrease in larval grow rate; mediate hosts. For example, the miracidium stage 3. an increase in the time to metamorphosis (with that infects a snail host can asexually replicate itself potentially increased exposure to planktonic to generate thousands of cercariae, the next stage predators); and in the life history. The extent of asexual reproduc- 4. a decrease in juvenile size. tion in these larval stages can vary widely due to The extent to which any fitness trade-off varies taxonomic group (Rohde, 1982, p. 54) and a num- among different forms of asexual reproduction by ber of interrelated life history factors summarized larvae is unknown. However, it seems reasonable by Poulin (2007), including host size and infec- to assume that any cost is correlated with two fac- tion longevity (Keeney et al., 2008), competition tors: (1) when asexual reproduction occurs dur- (Hendrickso­n and Curtis, 2002), and adult size or ing a species’ life history and (2) the proportion of longevity (Moore, 1981). the primary individual’s body that is allocated to In schistosome species, the extent of asexual re- cloning. Cloning by budding removes the smallest production in the miracidium stage is an appar- volume of material from the parent larva, and we ent trade-off with production, where larger hypothesize that this form of asexual reproduction embryos have higher asexual reproduction rates has the smallest cost to the parent larva. Autotomy (Loker, 1983). The increased number of asexually of the preoral lobe or paratomy of the posterolateral produced individuals may represent one adaptive arm(s), in contrast, involves loss of a greater volume mechanism for increasing successful transmission of tissue and potentially results in a greater cost to to a second intermediate or terminal host, a step in the parent larva through a reduction of feeding ca- the life history which may occur at a low frequency pacity, loss of , or both. Yet the elements of due to of the current host or low encounter 76 Evolutionary Ecology of Marine Invertebrate Larvae rates with the next host. Asexual reproduction of completed metamorphosis to produce a benthic ju- endoparasitic larvae in hosts may also be a com- venile. A more extreme example of the regenerative mon strategy in other parasitic species, including potential of developmental stages of echinoderms the Edwardsiella lineata, where larval was described by Dan-Sohkawa et al. (1986). They cloning occurs and parasite number correlates with dissociated gastrula-stage embryos of the sea star host size (Reitzel et al., 2009). We can hypothesize Asterina pectinifera using osmotic, ionic, and physi- that larvae of nonparasitic species may be selected cal forces, and then followed the re-­aggregation for asexual reproduction due to similar trade-offs of the isolated cells (or groups of cells). From in the plankton, where different selection pressures the initial suspension of cells, a free-swimmin­g, (e.g., likelihood of predation, feeding environment, ­blastula-like embryo was established after ≈30 h probability of successful settlement) may result post-­dissociation. After 80–100 h post-dissociation,­ in positive selection for asexual reproduction in a bipinnaria-stage larvae were reconstructed. Tamura­ species-dependent manner. Discerning between po- et al. (1998) examined the morphological events tential selective factors will require a combination of secondary coelomogenesis and described two of laboratory experimentation and resolved phylo- different processes that created the “coelomic genetic relationships for closely related species with pouches.” In some larvae (37 of 62 individuals) a and without larval asexual propagation. coelomic pouch was established through processes reminiscent of enterocoelly (“enterocoel-like”­ coe- 5.8 Open Questions for Future Research lom formation), while in other individuals (22 of 62 individuals) were established by an ag- (1) Does asexual reproduction by cultured larvae offer a gregation of mesenchyme-like cells (“schizocoelic- window to natural phenomena or represent an induced like” coelom formation); three reconstructed larvae developmental response to unnatural environmental formed coeloms through both processes. Not all conditions? reconstructed larvae were developmentally nor- Production of asexual propagules in response to mal as some individuals developed a multiple or a environmental conditions or changes in conditions branched digestive system. (food abundance: Vickery and McClintock, 2000; (2) Does asexual reproduction occur in all groups of Eaves and Palmer, 2003; McDonald and Vaughn, echinoderms, but the frequency of occurrence in some 2010; possible predators: Vaughn and Strathmann, groups is too low to detect in samples from the field? 2008; Vaughn, 2009; 2010) are known from in vitro Among echinoderm species that produce devel- experiments. Consequently, it is not certain whether opmental stages that undergo asexual reproduc- examples of asexual reproduction by embryos or tion, only cloning larvae of some species of the larvae in culture represent natural phenomena or Asteroidea and the Ophiuroidea have been identi- are developmental events induced by culture con- fied from plankton samples. However, species of ditions. There is evidence provided by early work- the Echinoidea and Holothuroidea are known to re- ers (e.g., Gemmill, 1914; 1915; MacBride, 1918) that produce asexually in laboratory cultures. If asexual deviations from normal development (e.g., larvae reproduction occurs in all groups, but at a variable with multiple or no pore canals) could be induced and, in some cases, low frequency, then detection of by culture conditions. cloning by embryos or larvae in laboratory cultures Echinoderm embryos and larvae exhibit a tremen- where large numbers of individuals can be evalu- dous capacity for regeneration. Research has dem- ated is not surprising. A low frequency of occur- onstrated that bisected echinoderm larvae of sea rence coupled with rapid rates of clone formation stars (Pisaster ochraceus, , and Patiria (e.g., Vaughn, 2009) further reduces the likelihood miniata) and sea urchins (Dendraster excentricus and of detecting rare, fast-developmental events from Lytechinus variegatus) are capable of regrowing the field samples. MacBride (1918) similarly com- excised portions of their body (Vickery and McClin- mented on the frequency of developmental abnor- tock, 1998; Vickery et al., 2002; Oulhen et al., 2016). malities in coelomogenesis of echinoderm larvae: In most cases, the regenerated larvae successfully “In this list of recorded instances of the occurrence Asexual Reproduction of Marine Invertebrate Embryos and Larvae 77 of two hydrocoels among echinoderm larvae, it will Luidiidae, order , Ophidiasteridae, order be noticed that only one such specimen was found , and Oreasteridae, order Valvatida), but among larvae fished from the open sea, although and species-level identities could not be re- hundreds of such larvae have been examined.” We solved. More recently, Galac et al. (2016) sequenced are hopeful that further field sampling will reveal mitochondrial and nuclear from cloning and the presence of cloning larvae of echinoids and aclonal bipinnariae and brachiolariae collected holothuroids. from the Florida Current of the Gulf Stream sys- (3) How does the ability of larvae to clone evolve in tem expressing the same color phenotype. Through marine invertebrate lineages? their analysis they assigned these specimens to a Currently, most descriptions of larval cloning single, yet undescribed, species within the family have been scattered throughout lineages, poten- Oreasteridae. Their species was equivalent to “Lar- tially due to opportunistic observations or studies val Group 1” reported by Knott et al. (2003). To our in species that can be cultured in the laboratory. If knowledge the only species of asteroid echinoderm asexual reproduction is a component of a life his- known to produce secondary larvae by paratomy tory that is under selection, we would expect it to is Luidia senegalensis (W. Jaeckle, personal observa- be gained and lost in lineages in the same way as tion). This specimen was identified based on the any other character. Research in gains and/or losses number of arm rays of the juvenile. of asexual reproduction in sea anemones (Geller (4) Will changing climate lead to increased asexual re- and Walton, 2001) as well as regeneration in an- production by larvae? nelids (Bely and Sikes, 2010) and other spiralians There is abundant evidence that climate change (Bely et al., 2014) suggest that these developmental will result in changes in ocean conditions that are processes can be quite dynamic within particular likely to have strong effects on microscopic larvae. lineages. The evolution of mechanisms of asexual Given what is known about abiotic induction of pol- reproduction requires explicit comparison in a re- yembryony and larval cloning (see earlier), there is solved phylogeny where the presence or absence of reason to believe that some potential outcomes of cli- “asexual reproduction” by embryos or larvae can mate change will also lead to increased frequency of be mapped to determine if this is a primitive or a asexual reproduction. First, phytoplankton blooms derived life history character. may shift in their frequency, intensity, and location In asteroids, current evidence hints that larval under future climate change scenarios. It is likely asexual reproduction may have evolved multiple these changes will be uneven and likely difficult to times. Cloning larvae have been collected from predict. For example, in the North Atlantic warming opportunistic sampling from Barbados, Panama, sea surface temperatures have resulted in both in- Beliz­e, Jamaica, Commonwealth of the Bahamas, creased (in cooler regions) and decreased (in warmer Gulf of Mexico, and throughout the Gulf Stream regions) phytoplankton abundance (Richardson and system. Despite this regional geographic distribu- Schoeman, 2004). If the overall levels of phytoplank- tion and high seasonal abundances (Knott et al., ton increase, or if the speed and intensity of bloom 2003), the species identity of cloning asteroid larvae appearance increase, current research (Vickery and remains poorly resolved. Using morphological fea- McClintock, 2000; McDonald and Vaughn, 2010) tures of collected larvae, Bosch et al. (1989) assigned suggests that larval cloning may be facilitated. cloning bipinnariae from the Sargasso Sea to the ge- Concurrent with ocean warming, there has also nus Luidia (order Paxillosida). Further samples from been a freshening of the surface waters where the the waters surrounding the Commonwealth of the development of marine invertebrates frequently Bahamas and from the Florida Current of the Gulf occurs. While freshening is not uniform globally, system revealed the presence of cloning larvae from major portions of the world’s oceans are freshening, a non-paxillosid group (Jaeckle, 1994). Knott et al. including the Gulf of Maine (notably on Georges (2003) compared tRNA sequences and recog- Bank), parts of the Indian and Pacific Oceans and nized three groups of cloning asteroid larvae (that the Southern Ocean (Wong et al., 1999; Drinkwa- nested among species of the taxonomic families ter et al., 2009; Haumann et al., 2016). Since at least 78 Evolutionary Ecology of Marine Invertebrate Larvae some cases of polyembryony are reported to oc- Acknowledgment cur in response to elevated temperature and con- comitant reductions in salinity (Allen et al., 2015), We acknowledge the assistance of Dr. Uwe Staerzfor­ it may be of special interest for developmental who provided a translation of Mortensen’s (1898) biologists and larval ecologists to examine field- description of “Auricularia paradoxa.” collected embryos and larvae for signs of polyem- AMR would like to thank the University of North bryony and cloning in areas where the interactive Carolina at Charlotte for support through a Junior effects of temperature rise and salinity decline may Faculty Development Award. be strongest. Greater understanding of the physi- ological tolerances and responses of embryos and References larvae, along with improved understanding of the mechanisms of asexual reproduction are needed Allen, J.D. 2008. Size-specific predation on marine inverte- before any substantive predictions can be made in brate larvae. Biological Bulletin 214: 42–49. this regard. Allen, J.D., Armstrong, A.F., and Ziegler, S.L. 2015. Envi- ronmental induction of polyembryony in echinoid echi- noderms. Biological Bulletin 229: 221–231. 5.9 Summary Alvarado, A.S. 2000. Regeneration in the metazoans: why does it happen? BioEssays 22: 578–590. 1. Larvae in multiple phyla of marine invertebrates Balser, E.J. 1998. Cloning by ophiuroid echinoderm larvae. undergo asexual reproduction, with most obser- Biological Bulletin 194: 187–193. vations occurring under laboratory conditions. Bely, A.E. and Sikes, J.M. 2010. Latent regeneration abili- 2. Echinoderms, particularly asteroids and echi- ties persist following recent evolutionary loss in asexual noids, are the most thoroughly described group . 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