Between a whale bone and the deep blue sea: the provenance of dwarf males in whale bone-eating tubeworms

When researchers first caught a glimpse of the lush carpet of pink tubeworms covering the scattered bones of a dead grey whale 2900 m below the surface of Monterey Bay, the excitement onboard the Western Flyer (the mother ship of the remotely operated vehicle the Tiburon) must have been electrifying. The discovery of a new genus and several species of whale bone-eating Osedax tubeworms (Annelida, Siboglinidae) a mere 6 years ago from the deep sea was itself noteworthy. But what the researchers peering into the video monitors aboard the Western Flyer could not have known at that moment was that in the gelatinous tubes of those worms clung even more peculiar forms: harems of tiny, paedomorphic males of Osedax, numbering in the hundreds at times. Whereas female tubeworms bore into the marrow of whale bones (possibly via enzymes from their endosymbiotic bacteria), the dwarf males secondarily colonize the tubes of the resident females. The number of males in a female's tube increases over time in a curvilinear fashion. Dwarf males are known from all Osedax species examined to date, yet the origin of the males was an open question. In this issue, Vrijenhoek et al. provide compelling evidence that dwarf males found in the tubes of female Osedax worms are derived from a common larval pool and are unlikely to be the sons of host females or the progeny of females in the local genetic neighbourhood. This study provides an important foundation for future work on the ecology and evolution of extreme male dwarfism in Osedax and sexual size dimorphism more generally.     

Marine worms (genus Osedax) colonize cow bones

Bone-eating worms of the genus Osedax colonized and grew on cow bones deployed at depths ranging from 385 to 2893m in Monterey Bay, California. Colonization occurred as rapidly as two months following deployment of the cow bones, similar to the time it takes to colonize exposed whalebones. Some Osedax females found on the cow bones were producing eggs and some hosted dwarf males in their tubes. Morphological and molecular examinations of these worms confirmed the presence of six Osedax species, out of the eight species presently known from Monterey Bay. The ability of Osedax species to colonize, grow and reproduce on cow bones challenges previous notions that these worms are 'whale-fall specialists.'     

Acquisition of dwarf male "harems" by recently settled females of Osedax roseus n. sp. (Siboglinidae; Annelida)

After the deployment of several whale carcasses in Monterey Bay, California, a time-series analysis revealed the presence of a new species of Osedax, a genus of bone-eating siboglinid annelids. That species is described here as Osedax roseus n. sp. It is the fifth species described since the erection of this genus and, like its congeners, uses a ramifying network of "roots" to house symbiotic bacteria. In less than 2 months, Osedax roseus n. sp. colonized the exposed bones of a whale carcass deposited at 1018-m depth, and many of the females were fecund in about 3 months post-deployment. As with other Osedax spp., the females have dwarf males in their tube lumens. The males accrue over time until the sex ratio is markedly male-biased. This pattern of initial female settlement followed by gradual male accumulation is consistent with the hypothesis that male sex may be environmentally determined in Osedax. Of the previously described species in this genus, Osedax roseus n. sp. is most similar to O. rubiplumus, but it has several anatomical differences, as well as much smaller females, dwarf males, and eggs. Osedax roseus n. sp. is markedly divergent (minimally 16.6%) for mitochondrial cytochrome oxidase subunit I (mtCOI) sequences from any other Osedax species.     

Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla)

We explored two hypotheses related to potential differences between sexes in dispersal behaviour in western lowland gorillas (Gorilla gorilla gorilla). Direct observations suggest that immature females have more opportunities to move between breeding groups than immature males. The distribution of kin dyadic relationships within and between groups does not, however, support this hypothesis. At larger geographical scales, dispersal is likely to be easier for males than females because of the solitary phase most blackbacks experience before founding their own breeding group. However, previous work indicates that males settle preferentially close to male kin. By specifically tracing female and male lineages with mitochondrial and Y-chromosomal genetic markers, we found that male gorillas in the 6000 km2 area we surveyed form a single population whereas females are restricted to the individual sites we sampled and do not freely move around this area. These differences are more correctly described as differences in dispersal distances, rather than differences in dispersal rates between sexes (both sexes emigrate from their natal group in this species). Differences in resource competition and dispersal costs between female and male gorillas are compatible with the observed pattern, but more work is needed to understand if these ultimate causes are responsible for sex-biased dispersal distances in western lowland gorillas.     

Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms

We investigated the genetic diversity of symbiotic bacteria associated with two newly discovered species of Osedax from Monterey Canyon, CA, at 1,017-m (Osedax Monterey Bay sp. 3 "rosy" [Osedax sp. MB3]) and 381-m (Osedax Monterey Bay sp. 4 "yellow collar") depths. Quantitative PCR and clone libraries of 16S rRNA gene sequences identified differences in the compositions and abundances of bacterial phylotypes associated with the newly discovered host species and permitted comparisons between adult Osedax frankpressi and juveniles that had recently colonized whalebones implanted at 2,891 m. The newly discovered Osedax species hosted Oceanospirillales symbionts that are related to Gammaproteobacteria associated with the previously described O. frankpressi and Osedax rubiplumus (S. K. Goffredi, V. J. Orphan, G. W. Rouse, L. Jahnke, T. Embaye, K. Turk, R. Lee, and R. C. Vrijenhoek, Environ. Microbiol. 7:1369-1378, 2005). In addition, Osedax sp. MB3 hosts a diverse and abundant population of additional bacteria dominated by Epsilonproteobacteria. Ultrastructural analysis of symbiont-bearing root tissues verified the enhanced microbial diversity of Osedax sp. MB3. Root tissues from the newly described host species and O. frankpressi all exhibited collagenolytic enzyme activity, which covaried positively with the abundance of symbiont DNA and negatively with mean adult size of the host species. Members of this unusual genus of bone-eating worms may form variable associations with symbiotic bacteria that allow for the observed differences in colonization and success in whale fall environments throughout the world's oceans.     

Seasonal population dynamics of Pallisentis (Neosentis) celatus (Acanthocephala: Quadrigyridae) in the intestine of the rice-field eel Monopterus albus in China

Studies on the seasonal population dynamics of Pallisentis (Neosentis) celatus (Acanthocephala: Quadrigyridae) in the intestine of the rice-field eel Monopterus albus from the paddies and ditches in the Dong-ting Lake basin of China, were carried out with samples taken from June 2002 to May 2003. Prevalences were above 21% in all seasons sampled and with a distinct seasonal trend, which was highest (45.81%) in the spring and decreased by degrees. The mean intensity of infection was above 4.0 worms per fish. The maximum intensity of worms recovered from a single fish was 86 in the autumn of 2002. No significant seasonal differences were found in mean intensities, and differences in the mean abundance between winter and spring, winter and autumn were significant. Over-dispersed distributions of P. (N.) celatus in the host population, due to heterogeneity and feeding habits, were observed in all seasons. The size composition of both sexes of P. (N.) celatus showed males between 2.0 mm and 14.0 mm and females between 2.2 mm and 22.2 mm, with the main recruitment phase in the worm populations occurring in the summer and autumn, especially in the autumn, with the lowest recruitment occurring in the winter. The maturation and copulation of worms were mainly focused in the spring season. The sex ratio of female to male was both high in summer (1.09:1) and autumn (1.08:1). The higher proportion of females and the change in the worm sex ratio in summer can be attributed to the reduced longevity of male worms. As immature male worms exhibit a higher proportion of the worm population than females in all seasons, further studies are needed to determine if such a situation compensates for the shorter life span of males.     

Seasonal population dynamics of Neoechinorhynchus qinghaiensis in the carp, Gymnocypris przewalskii przewalskii, from Qinghai Lake, China

Studies on the seasonal population dynamics of Neoechinorhynchus qinghaiensis (Acanthocephala: Neoechinorhynchidae) in its fish host Gymnocypris przewalskii przewalskii in the Qinghai Lake, China, were carried out with samples taken in May 1991, August 1992, November 1992 and February 1993. Prevalences were higher than 44% in all seasons. The mean intensity of infection was above 124 worms per fish. The maximum intensity of worms recovered from a single fish was 1402 in the autumn of 1992. Differences in the mean abundance, mean intensity and prevalence are not statistically significant relative to season and this is likely to be related to the stable temperatures recorded at the bottom of Qinghai Lake. Over-dispersed distributions of N. qinghaiensis in the host population, due to heterogeneity and feeding habits, were observed in all seasons. The size composition of both sexes of N. qinghaiensis showed males to be less than 3.5 mm and females between 0.5 and 4.25 mm, with the main recruitment phase in the worm populations occurring in the autumn, extending through winter and spring with the lowest recruitment occurring in the summer. The maturation and copulation of worms were mainly focused in the summer season. The sex ratio of female to male was both high in winter (1.51:1) and spring (1.48:1). The higher proportion of females and the change in the worm sex ratio in winter can be attributed to the reduced longevity of male worms. As immature male worms exhibit a higher proportion of the worm population than females in all seasons, further studies are needed to determine if such a situation compensates for the shorter life span of males.     

Transmission pattern and intraspecific competition as determinants of population structure in pinworms (Oxyurida: Nematoda).

The transmission pattern of Zonothrix columbianus (Nematoda: Oxyurida) in its host Tropisternus columbianus (Coleoptera: Hydrophilidae), an aquatic beetle, was studied to determine whether parasites were dispersed with their hosts and to examine the possible role of intraspecific competition in limiting population size. Beetles were sampled at regular intervals from fall 1986 through fall 1989 and examined for worms. Worms, absent in larval stages of the host, were uncommon in newly metamorphosed beetles and therefore probably do not infect adult stages until after they have dispersed; worms are not dispersed with the host. Prevalence reached its lowest points in spring and fall when newly metamorphosed beetles were most common, but it was near 100% for most of the year. Worms were uniformly distributed in the host population. Many hosts had exactly 1 male and 1 female worm; the high prevalence suggests that this infrahost population results from interference competition between males on the one hand and females on the other. Only 3 of 285 beetles contained more than 1 male. Females shared the host with members of the same sex more commonly than males, but females from hosts harboring more than 1 female had significantly fewer eggs than lone females in hosts. Numbers of adult stages of beetles were estimated during spring, summer, and fall of 1989 and were lower in early spring and late fall. Because worms do not disperse with hosts, the panmictic unit could be estimated from the number of infected beetles; this probably was about 50 individuals during the winter bottleneck.     

The cypris larvae of the parasitic barnacle Heterosaccus lunatus (Crustacea, Cirripedia, Rhizocephala): some laboratory observations

Heterosaccus lunatus parasitizes the portunid crab, Charybdis callianassa in Moreton Bay, Australia. With the host crabs maintained at 22.5 degrees C this sacculinid rhizocephalan released larval broods every 6-7 days. During July-August 1996 and particularly August 1999 such broods showed the change-over from male only larvae in the early broods to females only in the later broods. As the host crabs were maintained under similar aquarium conditions in both years it is concluded that the light/dark cycle is the principal cue triggering this larval sex reversal. Oogenesis in the parasite externa is somehow controlled to produce two different sized ova - male larvae develop from large ova and females from small ova. A working hypothesis outlining how sex is probably determined for the larvae of sacculinids is erected. H. lunatus is considered the ideal sacculinid for the further experimental work necessary to verify the proposed sex-determining mechanism and its control processes. Measurements of the maximum swimming speeds of H. lunatus male and female cyprids showed the larger males to be the faster in absolute terms (27.95 compared with 17.60 mm s(-1), respectively), however, the calculated relative speeds were almost identical at approximately 90 body lengths s(-1). Settlement experiments confirmed that female H. lunatus cyprids settle only on the gills of C. callianassa; these cyprids needed to be at least 2 days old before they were able to settle.     

Grape variety affects female but also male reproductive success in wild European grapevine moths

Abstract.  1. For insect herbivores the quality of the larval host plant is a key determinant of their fitness. Only little attention, however, has been given to the effects of plants on mating success of males and its consequence for the reproductive output of their mates. In addition, almost all the studies that have investigated the influence of host plants on herbivore fitness components have been done in the laboratory, and less is known of these effects in natural conditions.
2. Using the phytophagous European grapevine moth ( Lobesia botrana Den. & Schiff., Lepidoptera: Tortricidae), we tested the influence of grape cultivars as larval food on the probability of acquiring a mate for both sexes, and on the reproductive output of females and males.
3. Results from this study stress the importance of larval host plants on the reproductive success of both sexes. Larval diet differentially affected mating success and reproductive output of male and female moths. Fecundity, egg size, and egg hatchability were significantly different when larvae were fed on particular grape cultivars.
4. A given cultivar that is of poor quality for females is generally also of poor quality for males. A cultivar, however, could be suitable for females but not for males and vice-versa. Apparently, the nutrients required for adult reproduction are not necessarily the same for males and females.
5. The important conclusion from this study is that evaluating the differential effect of host-plant species on traits associated with reproductive success of herbivores requires that the effects on both sexes be taken into account.     

Sexual size dimorphism in the ontogeny of the solitary predatory wasp Symmorphus allobrogus (Hymenoptera: Vespidae)

Sex-specific patterns of individual growth, resulting in sexual size dimorphism (SSD), are a little studied aspect of the ontogeny related to the evolutionary history and affected by the ecology of a species. We used empirical data on the development of the predatory wasp Symmorphus allobrogus (Hymenoptera, Vespidae) to test the hypotheses that sexual differences of growth resulting in the female-biased SSD embrace the difference in (1) the egg size and the starting size of larva, (2) the larval development duration, and (3) the larval growth rate. We found that eggs developing into males and females have significant differences in size. There was no significant difference between the sexes in the duration of larval development. The relative growth rate and the food assimilation efficiency of female larvae were significantly higher than compared to those of male larvae. Thus, the SSD of S. allobrogus is mediated mainly by sexual differences in egg size and larval growth rate.     

Relative larval loss among females during dispersal of Lake Sturgeon (<Emphasis Type="Italic">Acipenser fulvescens</Emphasis>)

Mortality that occurs during larval dispersal as a consequence of environmental, maternal, and genetic effects and their interactions can affect annual recruitment in fish populations. We studied larval lake sturgeon (Acipenser fulvescens) drift for two consecutive nights to examine whether larvae from different females exposed to the same environmental conditions during dispersal differed in relative levels of mortality. We estimated proportional contributions of females to larval collections and relative larval loss among females as larvae dispersed downstream between two sampling sites based on genetically determined parentage. Larval collections were composed of unequal proportions of offspring from different females that spawned at upstream and downstream locations (~0.8 km apart). Hourly dispersal patterns of larvae produced from females spawning at both locations were similar, with the largest number of larvae observed during 22:00–23:00 h. Estimated relative larval loss did not differ significantly among females as larvae were sampled at two sites approximately 0.15 and 1.5 km from the last section downstream of spawning locations. High inter- and intra-female variation in larval contributions and relative larval loss between nights may be a common feature of lake sturgeon and other migratory fish species, and likely is a source of inter-annual and intra-annual variation in fish recruitment.     

Age,growth, and sex ratio among populations of least brook lamprey,Lampetra aepyptera,larvae: an argument for environmental sex determination

Synopsis Sex ratios of least brook lamprey,Lampetra aepyptera, larvae varied widely among 12 geographically-diverse streams of the eastern United States. The extremes were 29 and 71% male, and the proportion of males increased significantly with relative population density, which was estimated among the streams from the number of larvae collected per m2 of substrate. The skewed sex ratios were not likely due to differential mortality between the sexes or differential recruitment to the adult stock, since they were established at the time of gonadal differentiation (at ca. 2 years of age) and remained relatively constant over the subsequent 2–3 years of larval life. Furthermore, although females seemed to predominate in the oldest larval age class, thus appearing to metamorphose later than males, their numbers were small and were omitted from the overall sex ratio. Sex ratio did not vary significantly with water hardness, pH, annual thermal units, or latitude. The possible adaptive significance of density-dependent sex determination in lampreys, however, remains elusive. It has been proposed that growth-promoting conditions might yield female-biased sex ratios as a tactic for ensuring that relatively large individuals become females, thereby increasing their fecundity. As predicted, larval size at a given age was generally greater in low-density populations, but there was no relationship between sex ratio and larval size, and female larvae were not consistently larger than the males.     

Role of Volatile Semiochemicals in the Host and Mate Location Behavior of Mallodon dasystomus (Coleoptera: Cerambycidae)

Little is known of the role semiochemicals play in the mating systems of longhorned beetles (Coleoptera: Cerambycidae) in the primitive subfamily Prioninae. Mallodon dasystomus (Say), the hardwood stump borer, is a widely distributed prionine native to the southern US. Preferred hosts of M. dasystomus include oak, sweetgum, sugarberry and hackberry; although they also colonize a variety of other hardwoods. Here, we study the mate location behavior of M. dasystomus by testing the hypotheses that the sexes are mutually attracted to volatiles emanating from the larval host and that females release a volatile pheromone that is attractive to males alone. In a Y-tube olfactometer, male and female M. dasystomus responded to volatiles from host material (i.e., sweetgum and sugarberry). However, only males responded to females in the olfactometer, suggesting that females release a volatile sex pheromone. In choice experiments conducted in a greenhouse, we determined that both males and females prefer host over non-host material. In further bioassays in the greenhouse, males chose host material containing a live female over that containing a live male or host material alone. These findings are further evidence of the critical role host volatiles and pheromones play in mating systems of longhorned beetles.     

High symbiont diversity in the bone-eating worm Osedax mucofloris from shallow whale-falls in the North Atlantic

Osedax worms are whale-fall specialists that infiltrate whale bones with their root tissues. These are filled with endosymbiotic bacteria hypothesized to provide their hosts with nutrition by extracting organic compounds from the whale bones. We investigated the diversity and distribution of symbiotic bacteria in Osedax mucofloris from shallow-water whale-falls in the North Atlantic using comparative 16S rRNA sequence analysis and fluorescence in situ hybridization (FISH). We observed a higher diversity of endosymbionts than previously described from other Osedax species. Endosymbiont sequences fell into eight phylogenetically distinct clusters (with 91.4-98.9% similarity between clusters), and considerable microdiversity within clusters (99.5-99.7% similarity) was observed. Statistical tests revealed a highly significant effect of the host individual on endosymbiont diversity and distribution, with 68% of the variability between clusters and 40% of the variability within clusters explained by this effect. FISH analyses showed that most host individuals were dominated by endosymbionts from a single cluster, with endosymbionts from less abundant clusters generally confined to peripheral root tissues. The observed diversity and distribution patterns indicate that the endosymbionts are transmitted horizontally from the environment with repeated infection events occurring as the host root tissues grow into the whale bones.     

Ecological disjunction across the sexes in an alloparasitoid: Host requirements,sex ratios and mate localization (Hymenoptera: Aphelinidae)

The larval females of Coccophagus sp. nr gurneyi Compere are primary parasitoids of lantana mealybugs, whereas males develop hyperparasitically through other parasitoids (never their own females), so the species is alloparasitic. Males are seldom even reared from lantana mealybugs (<0.3%, n = 4,212), and have not yet been reared from any other host. Adults were sampled in the field to establish that this species is sexual (by assessing female spermathecal content), and to quantify relative abundance of the sexes around host infestations. Adult males were scarce above hosts (3%, n = 314), but were attracted in relatively high numbers to caged virgin females within those infestations. Caged females outside infestations did not attract males, suggesting that mate attraction requires environmental signals other than those from females. Most females collected in the field above host infestations had sperm in their spermathecal capsules. They presumably had mated with males that developed elsewhere (so mate localization might involve searching across substantial distances). Virgin females were present only early in the day and evidently mate soon after eclosion. Evidence of sperm depletion in mated females was not found. The spatial scale of male and female movements needs to be quantified, but the ongoing movement of individuals (as a consequence of their sex‐related host relationships) seems to be a regular aspect of their ecology. The spatial and temporal dynamics across the sexes illustrates that their abilities to localize one another for mating leaves the sexes free to diverge ecologically, and their sex ratios to vary.     

The influence of host sex on the L3 to L4 molt of Brugia malayi

Immunocompetent male mice are more susceptible to experimental infection with Brugia spp. than are females. Because permissive male SCID mice (severe combined immunodeficient mice), which lack T and B cells, also possess higher worm burdens, the mechanism is not solely immune mediated. Recovery of fewer adult worms from the female SCID mouse suggests that females do not provide sufficient nutrients for larval growth. This study assessed the potential of the female SCID mouse to support the L3 to L4 molt of Brugia malayi. Unexpectedly, worms grown in females molted at earlier time points of recovery than those harvested from males. This suggests that the early stage of development of B. malayi is delayed in the male murine host. To determine whether the effect of host sex on molting may be similar in humans, worms were cultured in media supplemented with serum from male or female donors. Worms grown in serum obtained from female donors exhibited a significantly higher percentage of complete molts over those cultured with serum from males. Host-derived molecules required for the L3 to L4 molt may be more abundant in the female, perhaps allowing the worms to survive a vulnerable developmental stage in a less permissive environment.     

Host sex preferences and transmission success by the water mite Unionicola foili (Acari: Unionicolidae) parasitic on the midge Chironomus tentans (Diptera: Chironomidae)

This study examined whether ecoparasitic larval Unionicola foili exhibited a sex bias when infecting laboratory populations of the host insect Chironomus tentans and whether an association with male or female midges increased the likelihood of larval mites returning to the aquatic habitat. When laboratory populations of C. tentans were exposed to larval U. foili, there was a higher prevalence of mites among female hosts at emergence (17 of 30 males vs. 25 of 30 females infected by mites). However, there was no significant difference in the distribution or abundance of larvae among infected male (mean = 2.3 larvae per host) and female (mean = 2.6 larvae per host) midges. Larval mites parasitizing both male and female chironomids were more likely to return to water than could be expected by chance. Mite larvae infesting female C. tentans were more likely to return to water when female hosts deposited egg masses in water, suggesting that oviposition plays an important role in cueing larvae parasitizing female midges to detach. The mechanism responsible for increasing the likelihood that mites parasitizing male hosts return to water remains unclear. Future studies will address the possibility of parasite-mediated changes in host behavior.     

Not whale-fall specialists, Osedax worms also consume fishbones

Marine annelid worms of the genus Osedax exploit sunken vertebrate bones for food. To date, the named species occur on whale or other mammalian bones, and it is argued that Osedax is a whale-fall specialist. To assess whether extant Osedax species could obtain nutrition from non-mammalian resources, we deployed teleost bones and calcified shark cartilage at approximately 1000 m depth for five months. Although the evidence from shark cartilage was inconclusive, the teleost bones hosted three species of Osedax, each of which also lives off whalebones. This suggests that rather than being a whale-fall specialist, Osedax has exploited and continues to exploit a variety of food sources. The ability of Osedax to colonize and to grow on fishbone lends credibility to a hypothesis that it might have split from its siboglinid relatives to assume the bone-eating lifestyle during the Cretaceous, well before the origin of marine mammals.