On the Advantages and Disadvantages of Larval Stages in Benthic Marine Invertebrate Life Cycles
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MARINE ECOLOGY PROGRESS SERIES Vol. 177: 269-297. 1999 Published February 11 Mar Ecol Prog Ser REVIEW On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles Jan A. Pechenik* Department of Biology, Tufts University, Medford, Massachusetts 02155, USA ABSTRACT: many benthic marine invertebrates develop by means of free-livlng, dispersive larval stages. The presumed advantages of such larvae include the avoidance of competition for resources with adults, temporary reduct~onof benthic mortality while in the plankton, decreased likelihood of inbreeding in the next generation, and increased ability to withstand local extinction However, the direct~onof evolutionary change appears generally b~asedtoward the loss of larvae in many clades, implying that larvae are somehow disadvantageous. Poss~bledisadvantages include dispersal away from favorable habitat, mismatches between larval and luvenile physiological tolerances, greater sus- ceptib~lityto env~ronmentalstresses, greater susceptibihty to predation. and vanous costs that may be associated with n~etanlorphosingin response to specific chemical cues and postponing n~etamorphosis in the absence of those cues. Understanding the forces responsible for the present distribution of larval and non-larval (aplanktonlc) development among benthic marine invertebrates, and the potential influence of human activities on the direct~onof future evolutionary change in 1-eproductlve patterns, will require a better understanding of the following issues. the role of macro-evolutionary forces in selecting for or against dispersive larvae, the relative tolerances of encapsulated embryos and free-liv- ing larvae to salinity, pollutant, and other environmental stresses; the degree to which egg masses, egg capsules, and brood chambers protect developing embryos from environmental stresses; the relative magmtude of predation by planktonic and benthic predators on both larvae and early juveniles; the way In which larval and juvenile size affect vulnerability to predators; the extent to wh~chencapsula- tion and brooding protect against predators; the amount of genetic change associated with loss of lar- vae from invertebrate life cycles and the time required to accomplish that change; and the degree to which continued input of larvae from other populations deters selection against dispersive larvae The prominence of larval development in modern life cycles may reflect difficulties In loslng larvae from llfe cycles more than selection for their retention. KEY WORDS. Larvae . Life cycle evolution. Marine invertebrates INTRODUCTION adults, they reach the juvenile stage through a con- spicuous metamorphosis (Giese & Pearse 1974, Hill The life cycles of most benthic marine invertebrate 1991, McEdward & Janies 1993, Nielsen 1998). Other species include microscopic, free-living dispersive reproductive patterns lack dispersive larval stages: stages that may be feeding (planktotrophic) or non- individuals develop to the juvenile stage entirely feeding (lecithotrophic).In this paper I refer to these within egg masses, egg capsules, or brood chambers, free-living developmental stages as larvae. Larvae are although they often pass through a distinctly larval morphologically and ecologically distinct from the morphology; I refer to such reproductive patterns as 'aplanktonic.' My definitions thus emphasize where prejuvenile development takes place rather than dif- ferences in developmental morphology. Jablonski & 0 Inter-Research 1999 Resale of full art~clenot permitted 270 Mar Ecol Prog Ser 177: 269-297, 1999 Lutz (1983), Grahame & Branch (1985), McEdward & lected for as developing embryos became increasingly Janies (1993),Havenhand (1995),and Levin & Bridges well adapted to their planktonic habitats (Jagersten (1995) discuss alternative terminologies. This paper 1972, Strathmann 1993, Wray 1995). That aplanktonic concerns the forces that may drive reproductive pat- development is often associated with substantial terns toward larval or aplanktonic development and behavioral and anatomical modification of adults (e.g. the constraints that may deter evolution from one pat- Fretter & Graham 1994, Byrne & Cerra 1996, Mooi & tern to the other. David 1996) also suggests a derived condition in at Of the approximately 40 animal phyla represented in least many clades, as does the occurrence of what the ocean, only nematodes, chaetognaths, gastrotrichs, seem to be vestigial larval organs (e.g.the velar lobes kinorhynchs, gnathostomulids, and tardigrades do not of developing gastropods) in the development of many include a morphologically or ecologically distinctive, aplanktonic species (Jagersten 1972, Hadfield & Iaea free-living dispersive larval phase in their life history 1989, Olson et al. 1993, Strathmann 1993, Byrne & (Strathmann 1985, Levin & Bridges 1995). Thorson Cerra 1996, Moran in press). (1950, 1966) estimated that 55 to 85% of all benthic Free-swimming larval stages have clearly been lost marine invertebrate species produce long-lived plank- one or more times within many groups, including gas- totrophic larvae (spending weeks to months in the tropods, echinoderms, and ascidians (e.g. Strathmann plankton), 5 % produce short-lived planktotrophic lar- 1978, Gallardo & Perron 1982, Raff 1987, 1996, Wray vae (spending hours to days in the plankton), and 1995, Arndt et al. 1996, Poulin & Feral 1996, Hart et al. about 10 % produce lecithotrophic larvae. Even if these 1997, Jeffrey 1997, McEdward & Janies 1997, Ponder & estimates should prove excessive in some groups as Lindberg 1997, Nielsen 1998). Larvae are unlikely more life histories are described (Giangrande 1997),it to be regained within a clade once lost, particularly seems safe to say that free-living larval development- when that loss has been accompanied by substantial particularly planktotrophic development-is at least morphological simplification during embryogenesis very common within the life cycles of benthic marine (McEdward & Janies 1997). McEdward (1992, 1995) invertebrates (Morgan 1995a) and that planktotrophic has documented what appears to be an intriguing development has persisted in many clades for hun- exception, the asteroid Pteraster fesselatus, which has dreds of millions of years (Wray 1995). Because so apparently evolved a morphologically unique, lecitho- many species produce dispersive larvae, it is generally trophic larva from a brooding ancestor. assumed that larvae have been selected for (reviewed The apparently biased tendency toward the loss of by de Beer 1958, Underwood 1974, Rex & WarCn 1982, larval stages from life histories in at least some clades Grahame & Branch 1985, Hedgecock 1986, Levinton suggests that larvae can be a liability, something that 1995, Wray 1995). However, certain apparent trends in selection has acted against. Dispersive larvae are life cycle evolution suggest that larvae have been unlikely to be lost in sessile species such as barnacles, selectively disadvantageous in many groups. but even here there has been selection for reduced dis- Although it is not certain whether early larvae were persal in some cases (e.g. Newman & Ross 1977, as feeding or nonfeeding (e.g. Rouse & Fitzhugh 1994, cited in Jablonski & Lutz 1983, p 44, Anderson 1994). Hadfield et al. 1997, Ponder & Lindberg 1997; re- Particularly among clonal animals selection has clearly viewed by Nielsen 1998), it is generally believed that favored retaining offspring near the parents (Jackson free-living larvae of some sort are primitive in marine 1986).Although there is growing understanding about invertebrate life histories and that the loss of larval the genetic mechanisms mediating the loss of larval stages is a derived condition (e.g. Berrill 1931, Jager- stages, particularly among ech~nodermsand ascidians sten 1972, Hoagland 1986, Jackson 1986, Strathmann (Swalla et al. 1993, Wray 1995, Raff 1996). the pres- 1986, Emlet et al. 1987, Raff 1987, 1996, Reid 1989, sures selecting for such loss are still unresolved Giangrande et al. 1994, Page 1994, Rawlings 1994, (reviewed by Grahame & Branch 1985, Emlet et al. Mooi & David 1993, Rieger 1994, Strathmann & 1987, Olson et al. 1993, Havenhand 1995, Wray 1995). Eernisse 1994, Havenhand 1995, Wray 1995, Bhaud & The apparent selection against dispersive larvae in DuchBne 1996, Byrne & Cerra 1996, Hart et al. 1997, at least some major marine invertebrate groups raises Ponder & Lindberg 1997, Nielsen 1998).This assump- two intriguing questions: (1)To what extent are larvae tion is supported by logical argument and intuition, d~sadvantageousin marine invertebrate life cycles? and by some cladistic analyses (e.g. Arndt et al. 1996, and (2) if the direction of evolutionary change has been Hart et al. 1997, Ponder & Lindberg 1997),rather than primarily toward the loss of larval stages, why is larval by direct evidence. If external fertilization is primitive, development still so common? This latter question or, as argued by Nielsen (1998), if the ancestral animal has been posed explicitly a number of times (e.g. Jack- life cycle was entirely planktonic, then it is easy to see son 1986, Havenhand 1995) but never thoroughly how morphologically distinctive larvae would be se- addressed. This review addresses both questions. Pechenik: Advantages a nd disadvantages of larvae 27 1 The ancestral nature of larvae has been questioned rare (Jablonski & Lutz 1983, Jablonski 1986, Levin & several times in the past dozen years. Chaffee & Lind- Bridges 1995, Chia et al. 1996, Krug