Biol. Bull. 211: 204-207. (December 2006)
© 2006 Marine Biological Laboratory
Maternal Provisioning in Ophionereis fasciata and O. schayeri: Brittle Stars With Contrasting Modes of Development
Inke Falkner1,*,
Maria Byrne1 and
Mary A. Sewell2
1 Department of Anatomy and Histology, F13, University of Sydney, 2006, Australia
2 School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand
* To whom correspondence should be addressed. E-mail: inke{at}anatomy.usyd.edu.au
 |
Abstract
|
|---|
Evolutionary change from planktotrophic to lecithotrophic development in echinoderms is closely tied to an increase in maternal provisioning. We provide the first data on the major energetic constituents in the eggs of two ophiuroids, the planktotroph Ophionereis fasciata (egg diameter 103 µm) and the lecithotroph O. schayeri (egg diameter 248 µm), to document changes in maternal investment associated with the switch to lecithotrophy in O. schayeri. Lipid classes in the eggs of the two species did not differ except for the presence of small amounts of wax esters in the eggs of O. schayeri. Production of a large egg in O. schayeri is mostly due to enhanced deposition of one energy-storage lipid, triglyceride. The eggs of O. schayeri are not simply scaled-up versions of the ancestral-type eggs of O. fasciata. The relationship between lipid and protein content and egg volume conformed to the relationship previously established for echinoderm eggs. Surprisingly, total lipid and protein data for the eggs of O. schayeri grouped with data for the eggs of planktotrophic echinoderms. The eggs of O. schayeri are small compared with those of other echinoderms with lecithotrophic development, and their energetic contents may approach the minimum provisions necessary to permit development without feeding.
Investigations into the significance of egg size and energy content to development and larval ecology have generated numerous comparative, energetic, and modeling studies, many of which focus on echinoderms (1–5). As is typical of marine invertebrates, echinoderms have dispersive larvae whose types show a distinct dichotomy based on the amount of maternal provisions and the feeding mode (6). Species with planktotrophic development produce many small oligolecithal eggs and have feeding larvae, whereas species with lecithotrophic development produce fewer large macrolecithal eggs and have nonfeeding larvae (6). In echinoderms, planktotrophic development is regarded as the ancestral state, and lecithotrophic development has evolved independently multiple times (7,8). Evolution of increased maternal reserves is considered to have been a prerequisite for the switch to lecithotrophy and subsequent loss of superfluous feeding structures (7).
Vance’s (1,2) life-history models relating reproductive efficiency to egg size in marine invertebrates predict that selection should favor a bimodal egg-size distribution, with the extremes in egg sizes and larval feeding modes being most stable. Recent modifications of the Vance model give some explanations for the continuum in egg-size distribution seen in many marine taxa (9,10). For instance, data from 132 planktotrophic and lecithotrophic ophiuroid species show a unimodal egg-size distribution centered on eggs intermediate in size between the two extremes noted for asteroids and echinoids (11). There are, however, no data on energy content in ophiuroid eggs that would help us interpret this egg-size pattern. Here we provide the first data on the type and quantity of lipids and proteins in ophiuroid eggs, focusing on Ophionereis species with contrasting modes of development.
Ophionereis fasciata Hutton, 1872, endemic to New Zealand, is a planktotrophic developer (egg diameter 103 µm) with a typical ophiopluteus (12). Ophionereis schayeri Müller & Troschel, 1844, endemic to Australia, is a lecithotrophic developer (egg diameter 248 µm) with a nonfeeding vitellaria larva (12). The eggs of both species are negatively buoyant, indicating a high protein content (13).
Comparison of the eggs of these congeneric species provides phylogenetically robust insights into the changes in oogenesis associated with the evolution of lecithotrophy. The possession of eggs with a diameter of 250–290 µm and nonfeeding development in O. schayeri prompts two questions: (1) Are the eggs of O. schayeri simply scaled-up versions of the small egg of O. fasciata? (2) Is the lipid and protein content in the eggs of this lecithotrophic ophiuroid fundamentally different from that documented for the eggs of other echinoderms with this mode of development?
Figure 1A shows TLC/FID chromatograms of total lipid extracts of the eggs of O. fasciata and O. schayeri. Overall the lipid classes in the eggs of the two species were similar, with triglyceride the major lipid class present. Triglyceride in the eggs of O. schayeri showed a double peak. Comparison to spiked samples with a tripalmitin (C16) standard indicated that the double peak consisted of triglyceride with different length C-chains. The eggs of O. fasciata lacked wax ester, which was present at low levels in the eggs of O. schayeri. Wax ester appeared to be an additional constituent in the eggs of the lecithotrophic developer.
View larger version (33K):
[in this window]
[in a new window]
|
Figure 1. Results of chemical analyses for eggs of Ophionereis fasciata and O. schayeri. (A) Chromatograms from thin layer chromatography with flame ionization detection (Iatroscan) of total lipid extracted from the eggs (15). Specimens were collected at Matheson’s Bay, Leigh, New Zealand (O. fasciata), and Little Bay, Sydney, Australia (O. schayeri). Eggs of more than one female were pooled because isolated females did not spawn by themselves (12). For each species, three replicate samples of three independent spawnings were analyzed: sample size = 500 eggs for O. fasciata and 35 eggs for O. schayeri. AH, aliphatic hydrocarbon; KET, ketone standard; TG, triglyceride; CHOL, cholesterol; AMPL, acetone-mobile polar lipids; PL, phospholipid; NLM, non-lipid material, WE, wax ester. (B) Content of lipids, by class, in eggs. Mean values were divided by the egg volume (4/3 *r3) to compare lipid content data independent of egg size. Total lipid was calculated by adding all lipid classes. (C) Proportion of energy-storage lipids (AH, aliphatic hydrocarbon; WE, wax ester; TG, triglyceride) and structural lipids (CHOL, cholesterol; AMPL + PL, acetone-mobile polar lipid + phospholipid) in eggs.
|
|
Ophionereis schayeri had a significantly higher total lipid content (
= 1276.56 ng; SE = 40.9; n = 9) than O. fasciata ( = 31.56 ng; SE = 2.79; n = 9). To allow comparison between eggs of different volumes, we calculated the lipid density (lipid content/egg volume). Lipid density in the eggs of O. schayeri ( = 162.33 µg/µl; SE = 5.67; n = 9) was 3 times greater than that in the eggs of O. fasciata ( = 59.95 µg/µl; SE = 4.81; n = 8) (Fig. 1B). This significant difference (nested ANOVA, P < 0.05; F(1,4) = 394.0) was solely due to a higher triglyceride concentration in the eggs of O. schayeri, which was 7 times greater than that in the eggs of O. fasciata ( = 123.04 µg/µl versus = 17.19 µg/µl). The density of other lipid classes, including aliphatic hydrocarbon (AH), cholesterol (CHOL), and acetone-mobile polar lipid and phospholipid (AMPL + PL), was similar in the eggs of both species despite their size difference (Fig. 1B). The eggs of O. schayeri were therefore not simply scaled-up versions of the ancestral-type eggs of O. fasciata. The evolutionary increase in energy content in O. schayeri eggs was largely accomplished by increased synthesis of triglyceride.
Triglyceride was the major energy-storage lipid in the eggs of O. fasciata (31%) and O. schayeri (76%) (Fig. 1C). Together with the aliphatic hydrocarbon (3%) and the wax ester (3%), energy-storage lipids constituted 82% of the lipid in the eggs of O. schayeri (structural lipids 18%, Fig. 1C). In contrast, energy-storage lipids constituted 38% of the lipid in the eggs of O. fasciata. Structural lipids, especially phospholipid (54%), were the major lipid component in the eggs of O. fasciata (62%) (Fig. 1C). Clearly the increase in the lipid content of O. schayeri eggs involved a disproportionate increase in energy-storage lipids. These may be used to support larval development or stored to provide for the transition to a feeding juvenile, as seen in Heliocidaris erythrogramma (13,14).
Total protein in O. fasciata and O. schayeri was 0.024 µg/egg and 0.43 µg/egg, respectively. It is not known if this difference is due to an increase in the major yolk protein (MYP) or in some other proteins that facilitate lecithotrophic development. When scaled to egg volume, the eggs of O. fasciata and O. schayeri contained the same amount of protein, = 42.42 µg/µl (SE = 8.22; n = 6) and = 44.80 µg/µl (SE = 2.59; n = 6), respectively. Thus the protein/lipid ratio in the eggs of the planktotroph O. fasciata was substantially higher (0.71) than that for the lecithotroph O. schayeri (0.28), as is characteristic of echinoderms with these contrasting modes of development (4).
The data for the eggs of Ophionereis species conformed to previous trends noted for lipid and protein contents in the eggs of asteroids and echinoids. Thus the quantities of lipid and protein in the Ophionereis eggs are similar to those observed for other echinoderms (Fig. 2). The egg lipid and protein data cluster in two distinct groups, with the left cluster being planktotrophic species and the right cluster being lecithotrophic species (Fig. 2). Interestingly, the lipid and protein data for Ophionereis eggs placed both species in the planktotrophic cluster (Fig. 2). At a diameter of about 250 µm, the eggs of O. schayeri are at the lower limit of egg sizes seen in other echinoderms with lecithotrophic development, so it is not surprising that their energy profile does not overlap with those of lecithotrophic asteroids and echinoids with larger eggs. Does this mean that the eggs of O. schayeri contain just enough energy to support development without feeding, or do ophiuroids use their lipids at a much lower rate, thereby leaving deposits for the early juvenile stage?
View larger version (12K):
[in this window]
[in a new window]
|
Figure 2. Lipid and protein data of Ophionereis eggs are fitted into the regression determined for echinoderm eggs (4,16). Previous data are entirely from asteroids and echinoids. Protein was quantified with a modified Bradford assay with bovine serum albumin as the standard (17). Data for both species cluster with the planktotrophs.
|
|
The evolution of a larger egg and lecithotrophic development in O. schayeri involved an increase in the triglyceride content already present in the eggs of an ancestral-type planktotrophic developer such as O. fasciata. This disproportionate increase in triglyceride and the appearance of small amounts of wax ester appear to be the most significant changes in the lipid and protein content in the eggs of O. schayeri. Compared to the eggs of other echinoderms, O. schayeri eggs appear to be energetically similar. Their increased lipid content, however, is due to enhanced deposition of triglyceride instead of the wax ester that is reported for asteroids and echinoids (13). Whether the increased lipid reserves in the eggs of O. schayeri are used for development or stored for the early juvenile stage is being examined in ongoing research.
|
Acknowledgments
|
|---|
C. Mora, L. Elia, and R. Morgan helped collect specimens; S. Bishop helped with lipid analyses; and the IBR (University of Sydney) provided facilities for the protein analyses. The research was funded by a grant from the Australian Research Council.
|
Footnotes
|
|---|
Received 18 April 2006; accepted 17 August 2006.
|
Literature Cited
|
|---|
- Vance, R. R. 1973a. On reproductive strategies in marine benthic invertebrates. Am. Nat. 107:339–361.[ISI]
- Vance, R. R. 1973b. More on reproductive strategies in marine benthic invertebrates. Am. Nat. 107:353–361.
- Emlet, R. B., L. R. McEdward, and R. R. Strathmann. 1987. Echinoderm larval ecology viewed from the egg. Pp. 55–136 in Echinoderm Studies, M.J. Jangoux and J.M. Lawrence, eds. Balkema, Rotterdam.
- Jaeckle, W. B. 1995. Variation in the size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development. Pp. 49–77 in Ecology of Marine Invertebrate Larvae, L. McEdward, ed. CRC Press, Boca Raton, FL.
- Levitan, D. R. 2000. Optimal egg size in marine invertebrates: theory and phylogenetic analysis of the critical relationship between egg size and development time in echinoids. Am. Nat. 156:175–192.
- Thorson, G. 1950. Reproductive and larval ecology of marine bottom invertebrates. Biol. Rev. 25:1–45.[Medline]
- Strathmann, R. R. 1978. The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:894–906.[ISI]
- Raff, R. A., and M. Byrne. 2006. The active evolutionary lives of echinoderm larvae. Heredity 97:244–252.[ISI][Medline]
- McEdward, L.R. 1997. Reproductive strategies of marine benthic invertebrates revisited: facultative feeding by planktotrophic larvae. Am. Nat. 150:48–72.[ISI]
- Levitan, D.R. 1996. Predicting optimal and unique egg sizes in free-spawning marine invertebrates. Am. Nat. 148:174–188.[ISI]
- Sewell, M. A., and C. M. Young. 1997. Are echinoderm egg size distributions bimodal? Biol. Bull. 193:297–305.[Abstract]
- Selvakumaraswamy, P., and M. Byrne. 2000. Reproduction, spawning, and development of 5 ophiuroids from Australia and New Zealand. Invertebr. Biol. 119:394–402.
- Villinski, J. T., J. C. Villinski, M. Byrne, and R. A. Raff. 2002. Convergent maternal provisioning and life-history evolution in echinoderms. Evolution 56:1764–1775.[ISI][Medline]
- Emlet, R.B., and O. Hoegh-Guldberg. 1997. Effects of egg size on postlarval performance: experimental evidence from a sea urchin. Evolution 51:141–152.
- Sewell, M. A. 2005. Utilization of lipids during early development of the sea urchin Evechinus chloroticus. Mar. Ecol. Prog. Ser. 304:133–142.
- Sewell, M. A., and D. T. Manahan. 2001. Echinoderm eggs: biochemistry and larval biology. Pp. 55–58 in Echinoderms 2000, M. Barker, ed. Swets & Zeitlinger, Lisse, The Netherlands.
- Bradford, M. M. 1976. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72:248–254.[ISI][Medline]
TOP
Abstract
Literature Cited
