Elena K. Kupriyanova

Variation in sperm swimming behaviour and its effect on fertilization success in the serpulid polychaete Galeolaria caespitosa

Summary Established models of fertilization kinetics in free-spawning marine invertebrates predict that fertilization success is dependent upon sperm swimming velocity. Despite the prevalence of these models, there are very few published tests of this assumption. To test this, the effects of sperm swimming characteristics on fertilization success were studied in Galeolaria caespitosa (Polychaeta, Serpulidae). Both sperm activity (% motility) and sperm swimming velocities were highly variable within this species. Sperm were motile for up to 6–7 h after activation; however, mean motility, swimming velocity and fertilization success decreased after 4 h. Eggs of G. caespitosa were fertilizable up to 10 h after spawning; however, the number of embryos resulting from fertilization by fresh sperm also decreased after 4 h. Sperm motility and velocity were not affected by water-soluble egg extracts. When gamete concentration, contact time, and age were held constant, fertilization success in G. caespitosa remained highly variable. Some of this variability was attributable to observed variability in sperm motility and velocity. Fertilization success was positively related to sperm velocity (P = 0.014), but there was no correlation between percent sperm motility and fertilization success (P = 0.85). Cross-fertilization experiments indicated that individual egg fertilizability and male-female compatibility also play an important role in determining the fertilization success and thus may obscure any effects of sperm motility.

Phylogenetic relationships within Serpulidae (Sabellida, Annelida) inferred from molecular and morphological data

We assessed phylogenetic relationships within Serpulidae (including Spirorbinae) using parsimony and Bayesian analyses of 18S rDNA, the D1 and D9−D10 regions of 28S rDNA, and 38 morphological characters. In total, 857 parsimony informative characters were used for 31 terminals, 29 serpulids and sabellid and sabellariid outgroups. Following ILD assessment the two sequence partitions and morphology were analysed separately and in combination. The morphological parsimony analysis was congruent with the results of the 2003 preliminary analysis by Kupriyanova in suggesting that a monophyletic Serpulinae and Spirorbinae form a clade, while the remaining serpulids form a basal grade comprising what are normally regarded as Filograninae. Bremer support values were, however, quite low throughout. In contrast, the combined analyses of molecular and morphological data sets provided highly resolved and well‐supported trees, though with some conflict when compared to the morphology‐only analysis. Spirorbinae was recovered as a sister group to a monophyletic group comprising both ‘filogranin’ taxa (Salmacina, Filograna, Protis, and Protula) and ‘serpulin’ taxa such as Chitinopoma, Metavermilia, and Vermiliopsis. Thus the traditionally formulated subfamilies Serpulinae and Filograninae are not monophyletic. This indicates that a major revision of serpulid taxonomy is needed at the more inclusive taxonomic levels. We refrain from doing so based on the present analyses since we feel that further taxon sampling and molecular sequencing are required. The evolution of features such as the operculum and larval development are discussed.

Naming species with no morphological indicators: species status of Galeolaria caespitosa (Annelida : Serpulidae) inferred from nuclear and mitochondrial gene sequences and morphology

Galeolaria caespitosa Lamarck, 1818 is an endemic, gregarious serpulid annelid, ubiquitous along the intertidal zone of southern Australia, occurring from Queensland to Western Australia. We sampled specimens across this range and utilised morphological features and sequences of mitochondrial (cytochrome-b) and nuclear (ITS2) markers to assess the taxonomic status of this morphospecies. No taxonomically significant morphological differences were observed across the range of G. caespitosa. However, the molecular data revealed the existence of the following two well supported clades that were also geographically concordant for the two markers: an eastern clade, consisting of New South Wales and southern Queensland samples, and a south-western group that encompassed samples from the rest of its range. The minimum pairwise distance between members of the two groups was more than 24% for cytochrome-b, with a maximum of 1% within-group variation. In addition, analysis of molecular variation showed a high proportion (97%) of the total variation distributed among the two groups, indicative of long-term isolation of the two clades. These results suggest that G. caespitosa comprises at least two cryptic species. Here, we discuss the merits of naming new Galeolaria species, given there were no consistent morphological differences detectable and the absence of details on the type locality for G. caespitosa. We conclude that a new species of Galeolaria is warranted and describe it here as G. gemineoa.

Effects of temperature on sperm swimming behaviour, respiration and fertilization success in the serpulid polychaete, Galeolaria caespitosa (Annelida: Serpulidae)

Summary This study examines effects of water temperature on sperm swimming velocity, longevity, respiration, and fertilization success in the free-spawning serpulid polychaete Galeolaria caespitosa. Temperature is expected to influence metabolic rates (and swimming speeds) of sperm, and may affect sperm swimming through the mechanical effects of changing water viscosity. To separate the physiological and mechanical effects of water temperature, viscosity and temperature were manipulated independently. Changes in water temperature significantly influenced fertilization success and duration of sperm activity. In the range 11–31°C peak fertilization rates (>80%) were observed at 21°C, the typical summer water temperature in the native habitat. Both lower and higher temperatures resulted in significantly lowered fertilization rates. Longevity experiments demonstrated a trade-off between sperm velocity and duration of activity: at 21°C high sperm velocity declined sharply within 4 h, reaching zero within 8 h; at 11°C sperm maintained reduced velocity for over 12 h. Thus, temperature influenced sperm longevity and fertilization success by directly affecting sperm swimming velocity. Both physiological and viscosity-induced components of temperature were shown to affect sperm swimming velocity and corresponding fertilization success in G. caespitosa. Lower water temperature also resulted in significantly lower respiration rates of G. caespitosa sperm. However, viscosity alone did not significantly affect sperm respiration, suggesting that sperm may not be capable of compensating for velocity changes due to increased viscosity. Studies examining sperm metabolism and physiological compensation are needed to understand how broadcasting organisms achieve high fertilization rates in a wide range of ambient temperatures.

Live history evolution in Serpulimorph polychaetes: a phylogenetic analysis

The widely accepted hypothesis of plesiomorphy of planktotrophic, and apomorphy of lecithotrophic, larval development in marine invertebrates has been recently challenged as a result of phylogenetic analyses of various taxa. Here the evolution of planktotrophy and lecithotrophy in Serpulimorph polychaetes (families Serpulidae and Spirorbidae) was studied using a hypothesis of phylogenetic relationships in this group. A phylogenetic (parsimony) analysis of 36 characters (34 morphological, 2 developmental) was performed for 12 selected serpulid and 6 spirorbid species with known reproductive/developmental strategies. Four species of Sabellidae were used in the outgroup. The analysis yielded 4 equally parsimonious trees of 78 steps, with a consistency index (CI) of 0.654 (CI excluding uninformative characters is 0.625). Under the assumption of unweighted parsimony analysis, planktotrophic larvae are apomorphic and non-feeding brooded embryos are plesiomorphic in serpulimorph polychaetes. The estimated polarity of life history transitions may be strengthened by further studies demonstrating an absence of a unidirectional bias in planktotrophy-lecithotrophy transition in polychaetes.

BARRIERS TO CROSS‐FERTILIZATION BETWEEN POPULATIONS OF A WIDELY DISPERSED POLYCHAETE SPECIES ARE UNLIKELY TO HAVE ARISEN THROUGH GAMETIC COMPATIBILITY ARMS‐RACES

Abstract Although there are theoretical reasons to suspect that gametic incompatibility may develop readily among populations of broadcast spawning marine invertebrates, there have been very few studies documenting geographic patterns of interpopulation incompatibility for any species. To address this we determined how successfully individuals of the intertidal serpulid polychaete, Galeolaria caespitosa, can cross-fertilize within and among populations from across temperate Australia. Fertilization assays revealed asymmetrical differences between very distantly located populations from different coasts, with near-complete incompatibility between eggs from Sydney with sperm from Adelaide, but the reverse cross (Adelaide eggs, Sydney sperm) was reasonably compatible. Although that pattern was congruent with a clear difference in Cytochrome B sequences between worms on the south and east coasts of Australia, we also detected some indication of interpopulation incompatibility within the genetic grouping on east coast, between two populations separated by only 220 km. We then assessed whether commonly proposed gametic compatibility arms-races could account for these patterns. Our results suggest reduced gametic compatibility may reduce a females maximum fertilization potential, resulting in a cost to this potential mechanism for reducing polyspermy. Consequently, the apparently rapid development of reproductive barriers here seems unlikely to have been driven by arms-races involving sexual conflict over fertilization rate.

Serpulidae (Annelida, Polychaeta) of the Arctic Ocean

Abstract This paper is an account of Serpulidae (Annelida, Polychaeta) collected from the Arctic and Northern Atlantic Oceans by Soviet expeditions. This material is part of the collection of the Department of Hydrobiology at Moscow State University and the Zoological Museum of the Russian Academy of Sciences in St. Petersburg. We redescribe eleven species: Chitinopoma serrula, Ditrupa arietina, Filograna implexa, Hyalopomatus claparedii, Hydroides norvegicus, Placostegus tridentatus, Pomatoceros triqueter, Protula globifera, P. tubularia, Protis arctica, and Serpula vermicularis. A new species from this collection, Metavermilia arctica, was described in a previous publication. Original illustrations and distribution maps accompany all descriptions. We provide two separate taxonomic keys to specimens and tubes. The previous records of arctic serpulids and the present state of the taxonomy of the family are discussed. Based on the operculum-bearing specimens of Protis arctica found, and on previous similar...

Evolution of the unique freshwater cave-dwelling tube worm Marifugia cavatica (Annelida: Serpulidae)

Abstract Of the approximately 350 described species of serpulid polychaetes, only Marifugia cavatica inhabits fresh water. It is distributed in ground waters of the Dinaric Karst in northeastern Italy, Slovenia, Croatia, and Bosnia and Hercegovina. Five other serpulid species, comprising the genus Ficopomatus, are found in brackish water locations worldwide; otherwise serpulids are all marine organisms. We re‐describe M. cavatica and examine the fine structure of its chaetae with SEM as well as summarise its distribution. The morphology of Marifugia provides an ambiguous indication of its phylogenetic relationships, thus DNA sequence data was also used. Phylogenetic analysis of nuclear rDNA 18S and 28S sequences using maximum parsimony, maximum likelihood and Bayesian analyses places Marifugia as a sister group to a clade of brackish‐water Ficopomatus species. Osmoconformity and penetration into non‐marine waters hence appears to have taken place once in the evolutionary history of Serpulidae. The transition to a subterranean environment may have occurred via ancestral marine shallow water to intertidal or estuarine species (like Ficopomatus) that evolved the necessary physiological mechanisms to withstand low salinity and then penetrated into freshwater caves via surface lakes.

Hydroides dianthus (Polychaeta: Serpulidae), an alien species introduced into Tokyo Bay, Japan

Calcareous tube polychaetes (family Serpulidae) are notorious biofoulers that are easily transported and introduced to allochthonous habitats. Here we report the recent introduction of Hydroides dianthus (Verrill, 1873) to eastern Japan as its first occurrence in East Asia, probably from European or American coasts. Specimens had been found on artificial hard substrata together with congeners H. ezoensis, H. exaltatus and H. fusicolus in Tokyo Bay, Japan in 2006. The origin, vector, source of introduction and possible impact of H. dianthus on Japanese coasts is discussed from a perspective based on worldwide Hydroides transport.

Evolution of a dense outer protective tube layer in serpulids (Polychaeta, Annelida)

Although the walls of most serpulid tubes are homogeneous, tubes of certain species may contain up to four ultrastructurally distinct layers. Some of these layers are made of densely packed large crystals and others are composed of sparsely packed fine crystals. In almost all (16 of 17) examined species having layered tubes, the dense layer is located in the outer wall part and the layer(s) composed of fine and relatively sparsely packed crystals are positioned in the inner wall part. Two species have transparent tube walls made entirely of densely packed crystals. Fossil serpulid tubes with dense outer layers (DOL) are known from the Late Cretaceous (Pentaditrupa subtorquata) and the Eocene (Pyrgopolon cf. mellevillei and Rotularia spirulaea). DOL gives a characteristic smooth shiny appearance to the tube surface and presumably evolved as an adaptation against drilling predation by gastropods and to delay shell dissolution in the waters of the deep-sea under-saturated with calcium carbonate..