BULLETIN OF MARINE SCIENCE, 48(2): 500-516,1991 SEXUAL REPRODUCTIVE MODES IN POLYCHAETES: CLASSIFICATION AND DIVERSITY W Herbert Wilson ABSTRACT A two-factor classification system for types of reproductive modes within the Polychaeta is described. The classification is based on the type ofIarval development and the fate of the female gametes (free-spawned or brooded in a variety of ways). A compilation ofinformation from the literature allowed the classification of 306 species. The Orders Phyllodocida and Spionida show the greatest diversity of reproductive modes. The most common reproductive mode involves the free spawning of gametes and the development of planktotrophic larvae. It is apparent that there has been multiple evolution of many reproductive modes during the course of polychaete evolution. This plasticity is argued to exceed that of the Classes Gas- tropoda, Bivalvia and Malacostraca. Polychaetes display an extraordinary diversity of reproductive traits (Schroeder and Hermans, 1975). It is not uncommon for congeneric species to possess rad- ically different means of reproduction. For example, the maldanid Axiothella mucosa produces gelatinous egg masses attached to the female tube (Bookhout and Hom, 1949). Sibling species of A. rubrocincta brood their young inside their tube and free spawn demersal eggs, respectively (Wilson, 1983). The plasticity of polychaete life histories has undoubtedly contributed to their success in the marine environment (Knox, 1977). Although a considerable literature exists on the reproductive traits of poly- chaetes (see references in Table 2), there has been no effort to survey the distri- bution of reproductive modes across orders and families. Fauchald (1983) divided polyaetes generally into three general reproductive life styles, although interme- diate species that are difficult to classify are common. My approach involves a finer classification of reproductive modes. Each class incorporates two aspects of reproduction. The first concerns the fate of the ova, particularly whether they are spawned freely into the seawater or afforded some type of brood protection or encapsulation. The second aspect concerns the type oflarval development: plank- totrophic (having planktonic feeding larvae), lecithotrophic (having planktonic, non-feeding larvae) or direct (having no free-swimming larval phase) (Thorson, 1950). The distribution of these modes across the orders and families of the Polychaeta are examined, using data from 306 species. MATERIALS AND METHODS I surveyed the literature for descriptions of the reproductive biology ofpolychaetes. To be classified in my scheme, information had to be provided on the fate ofthe ova (whether they are free-spawned or brooded) and the type of larval development (planktotrophic, lecithotrophic or direct). The clas- sification system that I have developed (Table 1) represents all combinations of six ova fate classes and the three larval development classes. The ova fate classes were developed based on my own knowledge of polychaete reproductive biology and are strictly applicable only to polychaetes. Each class is presumed to require specific morphological and physiological adaptations peculiar to that class, e.g., the ability to produce gelatinous egg capsules or the evolution of structures on the body for brooding. The larval developmental classes (Thorson, 1946; 1950) were selected a priori. These larval developmental classes can be applied to all marine invertebrates. The abbreviations given in Table I are used extensively in the text. The ova fate classes are: 1) free spawning, 2) brooding on the body, 3) brooding within the body (viviparity), 4) brooding in capsules within the tube, 5) brooding along the linings of the tube and 6) encapsulation in a gelatinous mass. The classification incorporates the notion of "mixed" development (Pechenik, 1979) in which embryos are sequestered for some portion 500 WILSON: POLYCHAETE REPRODUCTIVE MODES SOl Table I. List of the reproductive modes of polychaetes, based on the criteria of the fate of the ova and the type of larval development (Abbreviations for each mode are used throughout the text) Abbreviation Description FS-PLK Free spawning with planktotrophic larvae FS-LEC Free spawning with lecithotrophic larvae FS-DIR Free spawning with entirely benthic development BR-EXT-PLK Brooding on the outside of the body with release of planktotrophic larvae BR-EXT-LEC Brooding on the outside of the body with release of lecithotrophic larvae BR-EXT-DIR Brooding on the outside of the body with direct development BR-INT-PLK Brooding inside the body with release of planktotrophic larvae BR-INT-LEC Brooding inside the body with release of lecithotrophic larvae BR-INT-DIR Brooding inside the body with direct development BR-TUBE-PLK Brooding inside the tube with release of planktotrophic larvae BR-TUBE-LEC Brooding inside the tube with release of lecithotrophic larvae BR-TUBE-DIR Brooding inside the tube with direct development BR-CAP-PLK Brooding of encapsulated embryos inside the tube with release of plankto- trophic larvae BR-CAP-LEC Brooding of encapsulated embryos inside the tube with release of lecitho- trophic larvae BR-CAP-DIR Brooding of encapsulated embryos inside the tube with direct development GEL-PLK Encapsulation of embryos in a gelatinous mass with release of planktotrophic larvae GEL-LEC Encapsulation of embryos in a gelatinous mass with release of lecithotrophic larvae GEL-DIR Encapsulation of embryos in a gelatinous mass with direct development of early development in an encapsulating structure or other brood structure after which, in different species, the embryos may be released as planktotrophic larvae, as lecithotrophic larvae, or as benthic juveniles. I do not distinguish between the production of nurse eggs (exogenous yolk) and the production of endogenous yolk. There are numerous pathways for each (Eckel barger, 1988) and there is insufficient information to classify most species. The classification presented herein addresses only sexual reproduction and hence excludes the various types of asexual reproduction observed in polychaetes (Schroeder and Hermans, 1975). The larvae of some arabellid polychaetes are parasitic in other polychaetes (Richards, 1967); these are not considered in this paper. In reviewing the literature, I was able to find descriptions of the reproduction of 306 polychaetes which were sufficiently detailed to allow unambiguous classification of reproductive mode in my system. Many descriptions of other species had to be eliminated from the compendium because the investigators were unable to discriminate between planktotrophic and lecithotrophic larvae. Other descriptions did not indicate if early development involves free-spawned gametes or some type of brood protection. Nevertheless, the 307 species analyzed provide a summary of our knowledge of the distribution of reproductive modes across the higher taxa of the Polychaeta. The ordinal classification scheme given in Fauchald (1977) is used to group families; however, I do not consider his arrangement of orders to reflect polychaete phylogeny. Some families have received far more attention by repro- ductive biologists than other taxa; hence, better studied families may show a greater diversity of reproductive modes. Therefore, the 307 species classified do not constitute a random sample. This bias significantly reduces one's ability to make strong inferences about the relative diversities of reproductive modes between families and orders. RESULTS Table 2 presents the taxonomic compilation of polychaete species whose re- productive mode could be determined. For ease of search, taxa are arranged alphabetically; I make no assertion about polychaete phylogeny in this paper. The Amphinomida is listed first solely because this order comes first alphabetically, not because I consider it primitive. The 306 species classified belong to 36 families. Twenty-three species are classified into more than one category. Such plasticity may arise from geographic variation, from unrecognized sibling speciation or 502 BULLETIN OF MARINE SCIENCE, VOL. 48, NO.2, 1991 from poecilogony (Thorson, 1950). The reason for the variability is not important for purposes here; each mode represents a type found within the family and order to which the species belongs. Table 3 is a ranking of the frequency of occurrence of each reproductive mode from the data in Table 2. The FS-PLK mode (see Table I for a key to the abbreviations) occurs in 79 species, belonging to 22 families and seven orders. BR- TUBE-DIR is found in 39 species, distributed in II families and eight orders. FS-'LEC occurs in 34 species spread across 16 families and eight orders. Although BR-CAP-PLK is reported 24 times, all occurrences are in the family Spionidae. The next most common modes, BR-INT-DIR, GEL- LEC, BR-EXT-DIR and BR-CAP-DIR are spread across six, two, one and two order(s), respectively. The remaining modes are represented less than 15 times in the compilation. The only reproductive mode which is not represented at least once is BR-INT-PLK. A comparison of the orders well-represented in the compilation (Table 2) reveals that 9 reproductive modes are represented among the 21 species of the Order Capitellida. Within the order, four modes are found in the Arenicolidae (five species), seven modes are found in the Capitellidae (13 species) and four modes in the Maldanidae (eight species). Eight modes are found in the Order Eunicida with five modes in the Dorvilleidae (nine species)