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Worldwide Patterns in Mode of Development in Calyptraeid Gastropods

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Worldwide Patterns in Mode of Development in Calyptraeid Gastropods MARINE ECOLOGY PROGRESS SERIES Vol. 247: 103–122, 2003 Published February 4 Mar Ecol Prog Ser Worldwide patterns in mode of development in calyptraeid gastropods Rachel Collin1, 2, 3,* 1Committee on Evolutionary Biology, University of Chicago, Culver Hall, Room 402, 1025 E. 57th Street, Chicago, Illinois 60637, USA 2Department of Zoology, The Field Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA 3Present address: Smithsonian Tropical Research Institute, Unit 0948, APO AA 34002, USA ABSTRACT: The mode of development in marine invertebrates is believed to have consequences for dispersal, gene flow, geographic range, and speciation and extinction rates. The factors responsible for among-species differences in mode of development are not well understood and patterns of vari- ation in mode of development have not been documented for many groups. I present a compiled data set of developmental characters for 78 species of calyptraeid gastropods: 53 Crepidula, 9 Calyptraea, 11 Crucibulum and 5 other species. Analysis of this data set shows that egg- and hatching-size distri- butions are strongly positively skewed. As expected, egg size correlates with hatching size and time to hatching in species without nurse eggs. Egg size is not significantly different between species with planktotrophic development and species with direct development with nurse eggs. Hatching size of direct developers with and without nurse eggs do not differ. Developmental characters do not vary with adult body size among species. There are strong latitudinal effects in mode of development, the frequency of planktotrophic species decreases with increasing latitude while the proportion of direct developers increases. There is also a striking latitudinal pattern in the occurrence of nurse eggs; almost all species with nurse eggs occur in the southern hemisphere. These latitudinal patterns do not appear to be explained by sea surface temperature. Comparisons with other gastropods for which similar compilations are available show a striking difference between heterobranchs (opisthobranchs and pulmonates) and caenogastropods in developmental characteristics. KEY WORDS: Larvae · Invertebrate development · Crepidula · Crucibulum · Calyptraea Resale or republication not permitted without written consent of the publisher INTRODUCTION similar species with direct development (Scheltema 1989, Kohn & Perron 1994, but also see Ó Foighil 1989, Studies of a variety of marine invertebrates have Emlet 1995). These features are thought to result in shown that the type of embryonic and larval de- lower rates of speciation and lower rates of extinction velopment (direct or indirect, brooded, encapsulated for species with planktonic feeding larvae than for or planktonic) has far reaching evolutionary conse- species with direct, non-feeding development (e.g. quences. Species with planktonic developmental Hansen 1978, 1980, 1982, Strathmann 1985, Jablonski stages are thought to have higher rates of dispersal 1986a,b, 1987). and, therefore, higher rates of gene flow than species It is not clear what evolutionary factors lead to differ- with direct development (e.g. Berger 1973, 1977, ences in mode of development among species. How- Hedgecock 1982, McMillian et al. 1992, Duffy 1993, ever, patterns in mode of development appear to exist Hunt 1993, Hoskin 1997, Collin 2001). Mollusc and with latitude, habitat depth and body size (Thorson echinoderm species with planktonic planktotrophic 1946, 1950, Ockelmann 1965, Mileikovsky 1971, Strath- larvae also inhabit larger geographic ranges than mann & Strathmann 1982). Latitudinal patterns have *Email: [email protected] © Inter-Research 2003 · www.int-res.com 104 Mar Ecol Prog Ser 247: 103–122, 2003 been demonstrated for bivalve and gastropod faunas necessary data compilations are not widely available from the North Atlantic (Thorson 1950, Ockelmann for most groups of marine invertebrates. 1965) and the South American coast (Gallardo & The few existing compilations of data on gastropod Pencheszadah 2001); however, they have received development usually focus on a specific taxon and little attention in other geographic regions. Geo- often cover a small percentage of extant species. Per- graphic patterns of ascoglossan and nudibranch egg haps because they contain complete data for few taxa, size have been examined (Clark & Goetzfried 1978), most reviews of gastropod development (e.g. 38 spe- but geographic patterns of developmental characters cies of cephalaspids, Schaefer 1996; 53 species of muri- have not been closely examined for other, more exclu- cids, Spight 1976; 30 species of calyptraeids, Hoagland sive monophyletic groups of molluscs. Differences in 1986; have not been analyzed in as much detail as brooding and body size for sympatric pairs of species have the echinoid data. However, in-depth analysis were reviewed by Strathmann & Strathmann (1982), of development for 62 species of Indo-Pacific Conus but again, the available data are limited. Despite the (~15% of valid extant species; Kohn & Perron 1994) fact that these patterns have been demonstrated only showed that the mode and duration of development for geographically and taxonomically limited groups, correlate with egg size and that these characteristics they have provided the impetus for the development are associated with the size of a species geographic of various theories of the evolution of mode of de- range. Subsequently the same data were used by Duda velopment. For example, it has been proposed that & Palumbi (1999) to test the hypotheses that specia- seasonal productivity limits development at high tion rate is associated with mode of development. A latitudes to non-feeding development (e.g. Thorson large data set for opisthobranch molluscs (Hadfield & 1950), and that allometric constraints limit small Switzer-Dunlap 1984) shows that the egg size distri- animals to be brooders or produce embryos with bution of 260 species is not, as predicted by Vance non-feeding development (reviewed in Strathmann (1973a,b), bimodal and that duration of development, & Strathmann 1982). size at hatching and mode of development all correlate Basic comparative data on the reproductive charac- with egg size. The results from these 2 analyses both teristics of monophyletic groups of marine inverte- show significant associations between developmental brates are essential both to document patterns and to variables and egg size. However, the limited variation compare them with the patterns predicted by life his- in mode of development and geographic range of these tory modeling. Reviews and analyses of variation groups constrain the generalizations that can be made among species in reproductive and developmental from these 2 studies alone. For example, neither group characters are common for echinoderms (e.g. Mor- includes species with nurse eggs (where embryos tensen 1921, Emlet et al. 1987, Emlet 1990, 1995, Pearse developing from small eggs consume other eggs or 1994, Sewell & Young 1997). Developmental data com- embryos), a strategy common among caenogastropods pilations for echinoids include 204 species (24% of all (Spight 1976, Rivest 1983), and Conus is an entirely known echinoids and 45% of extant regular echinoids; tropical or sub-tropical genus. Emlet 1995), and egg-size data sets for other echino- Fifteen years ago, Hoagland (1986) published a derms include 149 species of asteroids, 132 species of review of development and reproduction of 30 species ophiuroids and 184 species of holothuroids (Sewell & in the caenogastropod family Calyptraeidae (both egg Young 1997). Such data compilations have been suc- size and hatching size for only 12 species). The present cessfully used to test Orton’s and Thorson’s ‘Laws’ paper builds on these data by reviewing information in (trends with depth and latitude; see Pearse 1994), more recently published papers and including previ- Vance’s prediction of a bimodal distribution of egg size ously unpublished observations. I use this data set to (Sewell & Young 1997), and the ideas that the size of a examine patterns of variation in mode of development species’ biogeographic range, body size and habitat as it relates to egg size, hatching size, female body size depth are associated with mode of development (Emlet and latitude. Specifically, I ask the following questions: 1995). In addition, comparative analyses have used Are the egg size and hatching size distributions right data from these compilations in combination with skewed and/or bimodal? How are egg size, hatching explicit phylogenies to investigate the patterns of evo- size and mode of development related? Is there a rela- lution of mode of development (Wray 1996, Cunning- tionship between body size and hatching size? Is there ham 1999). Because other invertebrate phyla show dis- a relationship between latitude or habitat temperature tinct types of development that are not present in and mode of development? This analysis provides a echinoderms, and because variation in mode of devel- data set and analyses similar to those already available opment often appears to be distributed differently for Conus (Kohn & Perron 1994) and for opisthobranchs among taxa in these groups, it is important to examine (Hadfield & Switzer-Dunlap 1984). Because all calyp- patterns in other invertebrate taxa. Unfortunately, the traeid species are protandrous hermaphrodites that Collin: Calyptraeid development 105 brood for the early portion of development and nurse For species that I have not
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