Rachel Collin

The effects of mode of development on phylogeography and population structure of North Atlantic Crepidula (Gastropoda: Calyptraeidae)

The mode of development of marine invertebrates is thought to influence levels of population structure and the location of species range endpoints via differences in dispersal ability. To examine these effects, populations of three sympatric clades of sedentary, marine gastropods in the genus Crepidula were sampled along the Atlantic and Gulf coasts of North America. A haplotype tree was constructed for each clade based on 640 bp sequences of mitochondrial cytochrome oxidase c subunit I. Examination of the tree topology, and amova analysis show that species with direct development (those hatching as benthic juveniles) have higher levels of population structure than do species with planktonic development. Both species in the direct‐developing C. convexa clade have high levels of geographical differentiation, with most populations representing a discrete clade of haplotypes. The planktotrophic species C. fornicata contains two major haplotype clades, both of which include samples from throughout the Atlantic coast. In this species there is no geographical differentiation among haplotypes but amova analysis detects a small but statistically significant level of geographical structure. The population structure within the C. plana species complex appears also to vary with mode of development: C. atrasolea, a direct‐developing species, has higher levels of population structure than does C. depressa, a sympatric planktotrophic species. The coincident occurrence of range endpoints and genetic breaks along the east coast of Florida in both direct‐developing species and species with planktonic development indicates that this biogeographic break is not due to development‐specific mechanisms such as hydrographic effects on larval recruitment.

Phylogenetic Relationships Among Calyptraeid Gastropods and Their Implications for the Biogeography of Marine Speciation

Although calyptraeid gastropods are not well understood taxonomically, in part because their simple plastic shells are the primary taxonomic character, they provide an ideal system to examine questions about evolution in the marine environment. I conducted a phylogenetic analysis of calyptraeid gastropods using DNA sequence data from mitochondrial cytochrome oxidase I (COI) and 16S genes and the nuclear 28S gene. The resultant phylogeny was used to examine the biogeographic patterns of speciation in the Calyptraeidae. Parsimony and Bayesian analyses of the combined data sets for 94 calyptraeid operational taxonomic units and 24 outgroups produced well-resolved phylogenies. Both approaches resulted in identical sister-species relationships, and the few differences in deeper topology did not affect biogeographic inferences. The geographic distribution of the species included here demonstrate numerous dispersal events both between the Pacific and Atlantic oceans and across the equator. When parsimony is used to reconstruct the movement from the Pacific to the Atlantic oceans on the phylogeny, there are 12 transitions between oceans, primarily from the Pacific to the Atlantic. When the latitude is coded as north versus south of the equator, the most-parsimonious reconstruction gives the origin of calyptraeids in the north followed by 15 dispersal events to regions south of the equator and no returns to the north. Many clades of the most closely related species are either sympatric or occur along a single coastline. Closely related species can, however, occur in such divergent regions as Southern California and South Africa. There is little evidence for sister-species pairs or larger clades having been split by the Isthmus of Panama or the Benguela upwelling, but the East Pacific Barrier appears to separate the most basal taxa from the rest of the family.

Dollo's law and the re–evolution of shell coiling

Gastropods have lost the quintessential snail feature, the coiled shell, numerous times in evolution. In many cases these animals have developed a limpet morphology with a cap–shaped shell and a large foot. Limpets thrive in marginal habitats such as hydrothermal vents, the high–energy rocky intertidal areas and fresh water, but they are considered to be evolutionary dead–ends, unable to re–evolve a coiled shell and therefore unable to give rise to the diversity seen among coiled snails. The re–evolution of a coiled shell, or any complex character, is considered unlikely or impossible (Dollos law) because the loss of the character is followed by the loss of the genetic architecture and developmental mechanisms that underlie that character. Here, we quantify the level of coiling in calyptraeids, a family of mostly uncoiled limpets, and show that coiled shells have re–evolved at least once within this family. These results are the first demonstration, to our knowledge, of the re–evolution of coiling in a gastropod, and show that the developmental features underlying coiling have not been lost during 20–100 Myr of uncoiled evolutionary history. This is the first example of the re–evolution of a complex character via a change in developmental timing (heterochrony) rather than a change in location of gene expression (heterotopy).

PHYLOGENETIC EFFECTS, THE LOSS OF COMPLEX CHARACTERS, AND THE EVOLUTION OF DEVELOPMENT IN CALYPTRAEID GASTROPODS

Abstract Despite considerable theoretical and empirical work on the population genetic effects of mode of development in benthic marine invertebrates, it is unclear what factors generate and maintain interspecific variation in mode of development and few studies have examined such variation in a phylogenetic context. Here I combine data on mode of development with a molecular phylogeny of 72 calyptraeid species to test the following hypotheses about the evolution of mode of development: (1) Is the loss of feeding larvae irreversible? (2) Is there a phylogenetic effect on the evolution of mode of development? (3) Do embryos of direct‐developing species lose the structures necessary for larval feeding and swimming and, if so, is the degree of embryonic modification correlated with the genetic distance between species? The results of these analyses suggest that mode of development evolves rapidly and with little phylogenetic inertia. There are three cases of the possible regain of feeding larvae, in all cases from direct development with nurse eggs. It appears that species with planktotrophic, lecithotrophic, or direct development with nurse eggs all have equal evolutionary potential and retain the possibility of subsequent evolution of a different mode of development. However, species with direct development from large yolky eggs appear to be subject to phylogenetic constraints and may not be able to subsequently evolve a different mode of development. Finally, species that have more recently evolved direct development have less highly modified embryos than older direct‐developing species. Since species with nurse eggs generally have fewer embryonic modifications than those from large yolky eggs, this embryological difference may be the underlying cause of the difference in evolutionary potential.

The slipper snail, Crepidula: an emerging lophotrochozoan model system.

Recent developmental and genomic research focused on “slipper snails” in the genus Crepidula has positioned Crepidula fornicata as a de facto model system for lophotrochozoan development. Here we review recent developments, as well as earlier reports demonstrating the widespread use of this system in studies of development and life history. Recent studies have resulted in a well-resolved fate map of embryonic cell lineage, documented mechanisms for axis determination and D quadrant specification, preliminary gene expression patterns, and the successful application of loss- and gain-of-function assays. The recent development of expressed sequence tags and preliminary genomics work will promote the use of this system, particularly in the area of developmental biology. A wealth of comparative information on phylogenetic relationships, variation in mode of development within the family, and numerous studies on larval biology and metamorphosis, primarily in Crepidula fornicata, make these snails a powerful tool for studies of the evolution of the mechanisms of development in the Mollusca and Lophotrochozoa. By bringing a review of the current state of knowledge of Crepidula life histories and development together with some detailed experimental methods, we hope to encourage further use of this system in various fields of investigation.

Molecular Phylogenetic and Embryological Evidence That Feeding Larvae Have Been Reacquired in a Marine Gastropod

Evolutionary transitions between different modes of development in marine invertebrates are thought to be biased toward the loss of feeding larvae. Because the morphology of feeding larvae is complex and nonfeeding larvae or encapsulated embryos with benthic development often have simplified morphologies, it is presumed to be easier to lose a larval stage than to reacquire it. Some authors have gone so far as to suggest that feeding larvae, morphologically similar to the ancestral feeding larvae, cannot be reacquired. However, the larval structures of some groups, most notably gastropods, are often retained in the encapsulated embryos of species that hatch as benthic juveniles. Therefore the re-evolution of feeding larvae using the same structures may be possible in these groups. Here we present the first well-substantiated case for the recent re-evolution of feeding larvae within a clade of direct-developers. DNA sequence data show that Crepipatella fecunda, a species of calyptraeid gastropod with planktotrophic development, is nested within a clade of species with direct development, and that Crepipatella dilatata, a species with direct development, appears to be paraphyletic with respect to C. fecunda. Observation of the embryos of C. dilatata shows that the features necessary for larval feeding and swimming are retained in the encapsulated veligers, suggesting that heterochronic shifts in hatching time and changes in nurse-egg allotment could have resulted in the re-evolution of feeding larvae in this species.

Phylogeography and bindin evolution in Arbacia, a sea urchin genus with an unusual distribution

Among shallow water sea urchin genera, Arbacia is the only genus that contains species found in both high and low latitudes. In order to determine the geographical origin of the genus and its history of speciation events, we constructed phylogenies based on cytochrome oxidase I and sperm bindin from all its species. Both the mitochondrial and the nuclear gene genealogies show that Arbacia originated in the temperate zone of the Southern Hemisphere and gave rise to three species in the eastern Pacific, which were then isolated from the Atlantic by the Isthmus of Panama. The mid‐Atlantic barrier separated two additional species. The bindin data suggest that selection against hybridization is not important in the evolution of this molecule in this genus. Metz et al. in a previous publication found no evidence of selection on bindin of Arbacia and suggested that this might be due to allopatry between species, which obviated the need for species recognition. This suggestion formed the basis of the conclusion, widely spread in the literature, that the source of selection on sea urchin bindin (where it does occur) was reinforcement. However, the range of Arbacia spatuligera overlaps with that of two other species of Arbacia, and our data show that it is hybridizing with one of them. We found that even in the species that overlap geographically, there are no deviations from selective neutrality in the evolution of bindin.

SEX RATIO, LIFE-HISTORY INVARIANTS, AND PATTERNS OF SEX CHANGE IN A FAMILY OF PROTANDROUS GASTROPODS

Abstract Application of optimality theory to the evolution of life histories has been broadly successful in predicting the conditions favoring sex change, the type of change, and the timing of such changes. The size advantage hypothesis predicts that the optimal size at which an individual should change sex is a function of its size and the size and sex of its potential mates. I collected data on the size, sex, and grouping of individuals of 27 populations of 19 species of the calyptraeids, a family of protandrous marine gastropods that includes Crepidula. These data are used to test the following predictions about variation in size at sex change: (1) sex ratio is biased toward the first sex; (2) the ratio of the size at sex change to the maximum size is a life‐history invariant; and (3) species that form variablesized groups or stacks have more variation in size at sex change than species that show less variation in stack formation. Across all 19 species, sex ratio was not significantly more often biased toward the first sex than it was toward the second sex, although sex ratios were significantly male biased more often than they were significantly female biased. Sex ratios ranged from 0.05 to 0.91, and this variation was related to mode of development, skew in size distribution, and frequency of stacking, but not with maximum body size. There was little evidence that the ratio of size at sex change and maximum size is invariant. There is evidence that one of the main underlying assumptions of this life‐history invariant, that male fertility increases with the same function of size in all species, is invalid for calyptraeids and probably for other animals. Finally, species that form larger stacks or mating groups had more variation in size at sex change within a population than species that were generally solitary. These results suggest that information about individual groupings should be included in predictions of life‐history theory and that more information about the relationship between male fitness and size is also needed.

Embryonic Velar Structure and Function of Two Sibling Species of Crepidula With Different Modes of Development

The structure and function of the embryonic velum of two closely related species of Crepidula with different modes of development are examined. The velum of C. dilatata, a direct developer whose embryos feed on nurse eggs, does not differ substantially from the velum of C. fecunda, a species with planktotrophic larvae. Although velar ciliation develops earlier in embryos of C. dilatata, embryos of both species were able to feed on small particles, using the opposed-band ciliary mechanism. However, the embryos of C. dilatata lose this ability as they grow. The embryos of C. dilatata were not able to swim, whereas those of C. fecunda swam consistently in vials of seawater. This difference in swimming ability is probably due to differences in velum-body size allometry between the two species.

Caribbean-wide, long-term study of seagrass beds reveals local variations, shifts in community structure and occasional collapse.

The CARICOMP monitoring network gathered standardized data from 52 seagrass sampling stations at 22 sites (mostly Thalassia testudinum-dominated beds in reef systems) across the Wider Caribbean twice a year over the period 1993 to 2007 (and in some cases up to 2012). Wide variations in community total biomass (285 to >2000 g dry m−2) and annual foliar productivity of the dominant seagrass T. testudinum (<200 and >2000 g dry m−2) were found among sites. Solar-cycle related intra-annual variations in T. testudinum leaf productivity were detected at latitudes > 16°N. Hurricanes had little to no long-term effects on these well-developed seagrass communities, except for 1 station, where the vegetation was lost by burial below ∼1 m sand. At two sites (5 stations), the seagrass beds collapsed due to excessive grazing by turtles or sea-urchins (the latter in combination with human impact and storms). The low-cost methods of this regional-scale monitoring program were sufficient to detect long-term shifts in the communities, and fifteen (43%) out of 35 long-term monitoring stations (at 17 sites) showed trends in seagrass communities consistent with expected changes under environmental deterioration.