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Evolutionary simplification of velar ciliation in the nonfeeding larvae of periwinkle (Littorina spp.).

The evolutionary loss of larval feeding has occurred multiple times in gastropods (e.g., 1, 2), with variable consequences for larval structures used to capture particulate food: in some cases, derived nonfeeding larvae retain structures used for food capture, but in others these are reduced or lost (2), (3). The fate of these structures in non-feeding larvae has implications for the potential re-evolution of larval feeding (4), (5). Larval feeding has been lost at least once in the genus Littorina, but nonfeeding larvae of some species in the genus retain the velum, using its marginal cells for endocytotic uptake of capsular albumen (3). Retention of the velum, one of whose main ancestral functions is particle capture, suggests that re-evolution of larval feeding might be possible in this group (5). We show that nonfeeding larvae of four Littorina spp. have lost the ciliary bands presumably used by their ancestors to concentrate planktonic food particles from suspension. Re-evolution of feeding in these larvae thus would require regaining opposed ciliary bands or other feeding structures. Acquisition of similar comparative data from other gastropod clades may help elucidate the conditions favoring loss of ancestral feeding structures in derived nonfeeding larvae.

The larvae of marine invertebrates are diverse in form and function, and biologists have long sought to understand the processes that generated this diversity. One compelling generalization is based on associations between larval nutritional mode and form. Larvae of some species must feed in the plankton in order to complete development, and these bear structures that function in particle capture and ingestion. Other larvae cannot feed in the plankton, because they lack functional feeding structures; instead, these larvae rely on materials stored in the egg (or otherwise maternally provided) to fuel development. Species with nonfeeding larval development and reduced or absent feeding structures have evolved many times from ancestors that had feeding larvae, which suggests that evolutionary loss of the requirement for feeding leads to the evolutionary loss of larval feeding structures (6).

However, there are exceptions to this scenario, some in the form of nonfeeding larvae that possess what seem to be ancestral feeding structures (e.g., 3, 5, 7). These cases are important in that they allow us to explore the conditions promoting loss of feeding structures and the timing of this process. Further, the re-evolution of larval feeding (typically considered a relatively rare event, with few clear cases identified) may be more likely in these lineages than in lineages with nonfeeding larvae that have completely lost feeding structures (e.g., 2, 4, 5).

Here we investigate a case in which feeding structures may have been retained after loss of feeding ability. The snail genus Littorina includes 18 extant species--8 with feeding larvae, and 10 with nonfeeding, fully encapsulated development (8), (9). Though relationships among these species are not completely resolved, existing phylogenies suggest that the common ancestor of the genus had feeding larvae, and that nonfeeding larvae arose only once in the genus, in the ancestor of the subgenus Neritrema (10).

The feeding larvae of Littorina spp., like those of all known feeding larvae of gastropods, capture food particles between two "opposed bands" of compound cilia (the prototroch and metatroch) borne on the edge of large velar lobes; particles are then carried to the mouth by short cilia in the gap between the opposed bands, the food groove (Fig. 1). Moran (3) showed that nonfeeding larvae of three Littorina spp. (L. saxatilis, L. sitkana, and L. subrotundata) retain large velar lobes and use them for a novel function--absorbing dissolved proteins from the capsular fluid. Using light microscopy, the author also showed that their velar lobes bore short cilia, but she did not describe the organization of these cilia. The extent to which structures involved in particle capture have been lost in nonfeeding larvae of Litlorina spp. is thus not yet clear. Those data are needed for making inferences about the likelihood of regaining larval feeding in members of this genus, and more broadly, for understanding the circumstances that lead to the loss of larval feeding structures following the evolutionary loss of larval feeding. Such data might also be useful for estimating rates of loss of larval feeding structures after the evolutionary loss of feeding in gastropods.

We examined the organization and behavior of velar ciliation in nonfeeding larvae of several species of Littorina, using light and scanning electron microscopy. Adults of three species with nonfeeding development were obtained from Lowes Cove, Maine (L. obtusata (Linnaeus, 1758)); San Francisco Bay, California (L. saxatilis (Olivi, 1792)); and Coos Bay, Oregon (L. sitkana Philippi, 1846). Adults of L. obtusata and L. sitkana deposited egg masses in the laboratory, and veligers of L, saxatilis were dissected from brooding females. Egg masses of a fourth species with nonfeeding development, L. subrotundata (Carpenter, 1864), were collected from a salt marsh in Coos Bay, Oregon. The four species we observed include three whose early stages are brooded in gelatinous masses, and one (L. saxatilis) whose embryos and larvae are brooded in the maternal oviduct. For comparison, we also examined the feeding larvae of two species of Littorina: L. keenae Rose-water, 1978, collected from San Pedro, California, and L. scutulata Gould, 1849. from Coos Bay, Oregon. These released egg capsules in the laboratory, and their larvae were reared for 1-3 weeks before examination. Using a compound microscope, we examined the velar cilia of living veligers of each species and estimated their lengths with a calibrated ocular micrometer. To visualize transport of particles along the edges of velar lobes, we added suspensions of unicellular algae to the preparations. For detailed descriptions of velar ciliation, we used scanning electron microscopy to examine whole larvae, and light microscopy for sectioned velar lobes.

As noted above, the velar lobes of the feeding larvae examined (those of L. keenae and L. scutulata) bore two bands of compound cilia (prototroch and metatroch) separated by an intermediate band of short food-groove cilia (Fig. 1). Prototrochal cilia were about 50 um in length in living larvae examined about 1 week after hatching. Larvae of the two species were essentially identical in velar form (only one, L. scutulata, is illustrated in Fig. 1). Direct observations of living larvae of these two species incubated in seawater with cells of the unicellular alga Rhodomonas sp. showed that algal particles were transported along the edges of the velar lobes to the mouth, as is typical for larvae that feed with opposed ciliary bands (11). Particles were presumably captured between prototrochal and metatrochal cilia beating in opposition, though we lacked the high-speed video camera needed to show this directly.

[FIGURE 1 OMITTED]

In contrast, the velar lobes of the four species of Littorina with nonfeeding larvae bore only short cilia (Tilde 10 um in length) on their edges (Fig. 2), as has been reported for three of the four species we observed (3). Previously unrecognized, however, was the fact that these cilia were not organized into the three ciliary bands characteristic of feeding larvae; instead, the velar edges of members of these four species bore only a single, wide band of short, simple cilia. These cilia arose from much larger epithelial cells (Tilde 30-40 /xm in height; Fig. 2) than did the prototrochal cilia of feeding larvae (Tilde 10-15 [um] in height; Fig. 1). In all of the nonfeeding larvae, all velar cilia appeared to beat in the same direction (anterior to posterior), and we saw no evidence of particle transport along the edges of the velar lobes to the mouth. The velar lobes of larvae of L. saxatilis, which are maternally brooded until metamorphosis, were very similar to those of larvae of the other three species, which develop to metamorphosis in gelatinous egg masses.

[FIGURE 2 OMITTED]

In general, the evolution of increased per-offspring maternal investment in lineages whose larvae were originally obligate feeders is thought to lead to the eventual loss of larval feeding structures and ability. Mechanisms proposed as responsible for the loss are relaxation of selection on feeding performance, selection for more rapid or efficient development to metamorphosis, or selection on feeding structures for alternative or novel functions (12), (13). However, these general conditions have yielded a diversity of endpoints in extant gastropods. In some species, nonfeeding larvae retain large velar lobes with opposed bands of cilia (e.g., 14, 15). In others, like the littorines described here, larvae retain large, distinct velar lobes, but the opposed ciliary bands often found on the edges of velar lobes are modified to form, for example, a single broad band or field (16). Finally, in some taxa the larvae either do not form velar lobes or produce lobes that are very reduced and lack opposed bands (17).

[ILLUSTRATION OMITTED]

In each case, the extent of modification in response to loss of the need for planktonic food is likely related to whether ancestral larval feeding structures are repurposed for functions other than food capture, and to the amount of time since loss of the requirement for larval feeding. Alternative functions that might promote the retention of opposed bands include the ingestion of particulate food provided by the mother (e.g., as intracapsular nurse eggs; 2, 4, 14, 15), though some species that feed on nurse eggs have lost their opposed bands (e.g., 16). Although nonfeeding larvae of littorines are not provided with nurse eggs, their capsules are provisioned with fluid that includes dissolved proteins; involvement of velar cells in the endocytotic uptake of these proteins (3) may have promoted retention of the velum. Dissolved proteins may increase the viscosity of the capsular fluid. Bending moments in such viscous capsular fluid would cause long cilia to buckle, perhaps driving the modification of typical opposed bands into the broader bands of short cilia found on the velar edges of the nonfeeding littorine larvae described here (3). Finally, velar cilia also contribute to larval movement within capsules, which has sometimes been suggested to enhance diffusion of oxygen to developing larvae (18).

Variation among lineages in the extent of modification of larval feeding structures may also reflect different lengths of time since loss of feeding. Collin (2), for example, showed that time since divergence (measured by the proxy of genetic distance) was somewhat correlated with "embryolog-ical divergence" between members of sister-species pairs of Crepidula spp. in which one species had planktonic, feeding larvae, and the other had nonplanktonic development. In that case, however, the measure of embryological divergence also included several traits, such as the presence of an operculum, that are not clearly related to larval feeding. In the littorines considered here, the timing of origin of the subgenus Neritrema (and, presumably, the loss of larval feeding) is poorly constrained, but one analysis suggests that it occurred roughly 4-10 mya (10, but see 9). Assuming a single origin of nonfeeding development in this clade, the similarity of the larvae of the four species examined here suggests two possibilities: (i) no changes in velar lobe morphology have occurred since the origin of the subgenus (despite several million years of evolution, including multiple speciation events and the acquisition of brooding in L. saxatilis); or (ii) increased maternal investment and encapsulation have led to convergence in velar form.

Strathmann (4) identified two pathways that might lead to the reacquisition of larval feeding in lineages of marine invertebrates in which larval feeding had been lost: (i) adultation--the repurposing in larval stages of structures originally used for feeding only in juveniles or adults; and (ii) the retention of ancestral larval feeding structures in nonfeeding larvae. No clear examples are known of gastropods regaining larval feeding by adultation (4). In at least some gastropods, the presence of velum and opposed bands in nonfeeding larvae represents retention of ancestral larval feeding structures. Similar retention of these ancestral structures has been suggested to have permitted re-evolution of larval feeding in several species of calyptraeid gastropods (5), (14). However, though members of Littorina (Neritrema) retain velar lobes as large as those of closely related species with feeding larvae (3), they have lost key components of the opposed-band system of particle capture. Together, these observations suggest that the reacquisition of larval feeding in their descendants is unlikely.

The loss of functional opposed bands in larvae of Litto-rina spp. is of particular interest because Reid (19), using phylogenetic inferences and data on protoconch morphology, suggested that larvae of several other littorines (Bern-bicium auratum and B. nanurn, Lacuna vincta, and Rissel-opsis varia) may have indeed regained larval feeding. Additional studies of phylogeny and of the functional morphology of members of these species and their relatives would allow stronger tests of the hypothesis of the re-evolution of larval feeding in these gastropods.

Acknowledgments

We thank A. Cohen, S. Lindsay, and M. Maliska for collecting various adult littorines for us. A. Moran kindly advised us on where to find specimens of L. subrotundata, and S. Maslakova provided lab space at the Oregon Institute of Marine Biology while we searched for adults and egg masses of that species. T. Douglass helped with equipment for sectioning, and SEM facilities were provided by the Institute for Integrated Research on Materials, Environment, and Society at CSU Long Beach. We thank R. Collin, R. Emlet, M. Maliska, R. Strathmann, and two anonymous reviewers for helpful discussions or useful comments on the manuscript. Support for this work was provided by a Scholarly and Creative Activities award from CSU Long Beach to B. Pernet.

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JEANETTE HOFSTEE AND BRUNO PERNET *

Department of Biological Sciences, California State University, Long Beach, 1250 BeUfiower Blvd, Long Beach, California 90840-3702

Received 16 July 2011; accepted 11 October 2011.

* To whom correspondence should be addressed. E-mail: Bruno. Pernet@csulb.edu
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Author:Hofstee, Jeanette; Pernet, Bruno
Publication:The Biological Bulletin
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Geographic Code:1USA
Date:Dec 1, 2011
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