Population genetic structure in brooding sea anemones (Epiactis spp.) with contrasting reproductive modes

Effects of dispersal and mating systems on the genetic structure of populations were evaluated by comparing five sea anemones: four Epiactis species that brood their offspring to the juvenile stage and one Anthopleura species that broadcasts gametes and has pelagic, planktotrophic larvae. The anemones were sampled at sites ranging from British Columbia to southern California between 1988 and 1992 and were analyzed by enzyme electrophoresis and by multilocus DNA-fingerprinting. Results were only partially consistent with expectations. While all four brooding species had lower observed heterozygosities than the broadcasting species, not all brooding species had greater population subdivision than the broadcasting species. The self-fertile E. prolifera had the expected evidence of intense local inbreeding ( f = 0.955); unexpectedly, the cross-fertile E. lisbethae and E. ritteri also had similar departures from random mating ( f = 0.957 and 0.831, respectively) probably due to biparental inbreeding among near neighbors in small, highly subdivided populations. Received: 24 May 1996 / Accepted: 12 July 1996     

The importance of biparental care in a precocial,monogamous bird,the bar-headed goose (Anser indicus)

Summary This study presents the first direct evidence of benefit derived from the male's parental effort during rearing of young in a monogamous, precocial bird species. We compared mothers accompanied by a mate (paired mothers) with single mothers, some of which were artificial widows, in a semicaptive flock of bar-headed geese (Anser indicus). Paired mothers were less often displaced by other birds and suffered fewer interruptions of brooding. Their goslings spent more time grazing and survived with a higher probability. Although one beneficial result of the male's parental effort may be the continued availability and survival of his mate, a more direct benefit arises from higher offspring survival between hatching and fledging.     

Genetic evidence of self-fertilization in the sea anemone Epiactis prolifera

Biochemical genetic variation provided evidence for the mode of reproduction of brooded young in the sea anemone Epiactis prolifera Verrill, 1869. Individuals of E. prolifera are female when small but hermaphroditic when large (i.e., gynodioecious); juveniles are brooded externally on the column. Brooding individuals collected from 6 intertidal sites (5 in central California and 1 in Washington State, USA) in the spring and summer of 1980 were assayed for gene-enzyme variation by starch-gel electrophoresis. Three of 12 enzyme loci were polymorphic; phosphoglucose isomerase appeared to be encoded by two, closely linked loci. Genotypic frequencies deviated markedly from expected random mating proportions. Only three heterozygotes were found; two were heterozygous at all three polymorphic loci, and the other was polymorphic at the two PGI loci. All 158 juveniles from 25 brooding individuals were assayed (2–19 juveniles per parent). Juveniles on homozygous adults were always identical to their parent. However, brooded young of heterozygous individuals were not identical to their parent. but showed 1:2:1 phenotypic segregation ratios consistent with reproduction by self-fertilization. This genetic evidence together with findings of marked heterozygote deficiencies and genetic identity of homozygous adults and their brooded young supports the conclusion that E. prolifera usually reproduces by self-fertilization, and cross-fertilization is rate.     

Comparing biochemical changes and energetic costs in gastropods with different developmental modes: <Emphasis Type="Italic">Crepipatella dilatata</Emphasis> and <Emphasis Type="Italic">C. fecunda</Emphasis>

The Chilean gastropods Crepipatella dilatata and C. fecunda have different development modes: brooding and direct development in C. dilatata and brooding and planktotrophic development in C. fecunda. Unlike many other congeneric invertebrate species pairs, recent genetic evidence suggests that C. fecunda may have evolved from C. dilatata. To explore the changes involved in this unusual evolutionary path, this study examined the biochemical, energetic, and morphological characters during early development of both species. Mean egg size was slightly smaller for the direct-developing species C. dilatata, and initial energy content was lower—by about 27%—for eggs of that species. In both species, protein content in the eggs was the principal biochemical component. Although females of C. fecunda produce 180 times more eggs than C. dilatata, females of C. dilatata invest 20 times more energy in each of their offspring, through nurse eggs; their embryos have approximately eight times more energy at hatching and about 5 times more energy when they enter the benthos, despite a long planktonic feeding period in the larvae of C. fecunda. Evolutionary switching between modes of development in these species is reflected in shifts in maternal energy investment.     

Brooding behaviour of the northern sea star Leptasterias polaris

The northern sea star Leptasterias polaris (Müller and Troschel) has a unique mode of brooding its young. The mother curves her arms along the plane of the disc, the whole individual assuming a flattened plate-like shape. In this form she covers the larvae, which are attached to the substratum beneath her. The central disc is not raised to form a brood chamber, as in related species, and there is no tendency to hide while brooding. In the St. Lawrence Estuary, brooding L. polaris are common from February through May and decline in numbers during June and early July. The genus Leptasterias originates in the Arctic and probably all species brood their young.This paper is dedicated to François Dorion who lost his life during benthic studies in the St. Lawrence Estuary. His enthusiasm in studying marine organisms will always be an inspiration to usContribution to the program of GIROQ (Groupe Interuniversitaire de Recherches Océanographiques du Québec)     

Reproductive patterns of scleractinian corals in the northern Red Sea

The majority of published accounts on scleractinian coral reproduction are from the tropical Pacific and Caribbean, with very little information known about Red Sea species. This report examines variation in reproductive mode in 24 species of hermatypic corals (belonging to seven families) in the Gulf of Eilat, Red Sea. Eighteen species are hermaphroditic broadcasters, two are hermaphroditic brooders and three are gonochoric broadcasters. In the Pocilloporidae, the gonads project into the body cavity, while in the other six families the gonads reside inside the mesenteries. The number of gonads per polyp in broadcasting species follows family or genus lines. Fecundity (eggs per polyp) increases with polyp size. Brooding species usually exhibit one or two gonads per polyp and each gonad contains only one to three oocytes. Oocyte size varies widely and does not relate to mode of reproduction. The largest oocytes (diameter = 450 μm) occur in the brooding coral Alveopora daedalea and in broadcasting species of the genus Acropora (diameter = 420 μm). Gonad morphology and gonochorism versus hermaphroditism appear to be constrained phylogenetically at the family or genus level. Lastly, this report compares the data presented for Red Sea scleractinian species with the data available on scleractinian corals from other geographical regions. Received: 2 February 1993 / Accepted: 9 March 1998     

Reproduction in the externally brooding sea anemone Epiactis georgiana in the Antarctic Peninsula and the Weddell Sea

External parental care is uncommon among actiniarians but common in Epiactis species. Here, several aspects of reproduction are analyzed for of one of them, Epiactis georgiana. Samples were collected in December, January, February, March, and April in the Antarctic Peninsula and the eastern Weddell Sea, during 1998, 2000, 2002, and 2003. Most sexually mature individuals of E. georgiana are male or female, but some are hermaphrodites. This is the first report of hermaphroditism in E. georgiana, which is the third species of the genus with this sexual pattern. The results suggest that oogenesis starts in December and that at least two generations of oocytes overlap; a third generation is often brooded externally. Putative fertilization is likely internal, and larvae and/or embryos are externally brooded on the distal part of the adult column until an advanced developmental stage. Apparently E. georgiana reproduces seasonally, probably releasing the embryos/larvae in the last months of the austral spring (December). Inter-individual variability was observed in gametogenesis. In addition, specimens from the Antarctic Peninsula were larger than those from the Weddell Sea. This study represents the first step in understanding the reproductive mode of E. georgiana.     

Genetic evidence for monogamy in the cooperatively breeding red-cockaded woodpecker

We examined the genetic relationship among putative parents, offspring, and helpers in 224 red-cockaded woodpeckers (Picoides borealis) from the Sandhills of North Carolina. Comparison of DNA similarity with a pedigree constructed from 3,823 individually-marked birds observed from 1979 to 1992 provided verification of observed relatedness in the sampled population (R ² = 0.87,df = 14,P<0.001). In this population, breeding pairs may or may not have helpers, most of which are males that remain on their natal territory. Our sample included helpers assisting their parents, helpers assisting a related male and an unrelated female, and helpers assisting an unrelated pair. Band by band comparison and examination of similarity among DNA profiles indicated that all offspring from non-helped nests were sired by their putative parents (n = 28 families). Similarly, all but one offspring in helped nests were also sired by their putative parents (n = 16 families). In the exceptional case, the offspring evidently was sired by a male external to the group. Analysis of similarity values supported the conclusion that matings by helpers or extra-group males are rare or non-existent. Our results indicate that in this species advantages gained by individuals remaining on their natal territories as helpers do not generally include siring offspring. Correspondence to: S. Haig     

Sexual reproduction of the solitary sunset cup coral Leptopsammia pruvoti (Scleractinia, Dendrophylliidae) in the Mediterranean. 2. Quantitative aspects of the annual reproductive cycle

There are few data on the reproductive biology of coral species living in temperate zones, particularly in the Mediterranean Sea. Leptopsammia pruvoti is a solitary coral that is commonly found in sea caves and under overhangs throughout the Mediterranean basin and along European coasts from Portugal to southern England. In this paper, we describe its annual reproductive cycle in the eastern Ligurian Sea near the city of Leghorn (Tuscany, Italy). Polyps were sexually mature at 3 mm in length (maximum diameter of the oral disc), were dioecious with a sex ratio of 1:1, and brooded their larvae. The maturation of spermaries took 12 months and oocytes 24 months. The rate of gonad development increased significantly from November to January, fertilization occurred from January to April and planulation during May and June. Seasonal variations in water temperature and photoperiod may have played an important role in regulating reproductive events. The amount of energy devoted to male gametogenesis (quantified by gonad index) was significantly higher in the sex separated species L. pruvoti than in the hermaphroditic dendrophylliid Balanophyllia europaea, whose reproduction has been studied in a previous work. We hypothesize that this difference is due to the contrasting sexuality or fertilization biology of these two species (cross-fertilization in the sex separated L. pruvoti versus possibly self-fertilization in the hermaphroditic B. europaea). Greater male sexual allocation in reproductive strategies characterized by dioecism or cross-fertilization when compared to those characterized by hermaphroditism or self-fertilization is common in plant mating systems. In relation to other solitary dendrophylliids, L. pruvoti presents an ‘r’-reproductive strategy.     

Reproductive habits and life cycle of the small clam Kingiella chilenica (Bivalvia: Cyamiidae) in an estuarine sand flat from the south of Chile

A population of the small clam Kingiella chilenica Soot Ryen 1959 was studied from March 1986 to December 1988 in an intertidal flat at Queule River, in the south of Chile. The life cycle and life history pattern of the bivalve were established contrasting population structure and dynamics to its reproductive habits. Individuals are gonochoristic and semelparous, presenting a typical annual life cycle. The species is a sequential brooder whose embryos undergo direct development. After the brooding season (summer through autumn), the adults disappear gradually (autumn through winter). Recruited juveniles overwinter during a relatively long period, undergoing rapid growth during the spring to attain the adult stage during the summer. The number of brooded embryos increases in proportion to adult length cubed. Life history traits of this bivalve are compared to those reported for other small brooder clams. Some basic tendencies become apparent when traits for semelparous versus iteroparous species are contrasted. As in other semelparous sequential brooders (Transennella tantilla, Gaimardia bahamondei), the relationship between brood size and shell length obseved in K. chilenica does not fit the allometry hypothesis for marine brooding invertebrtes that allometric constraints on the brooding space limit the fecundity of larger individuals. Also contrary to theoretical predictions, small body size does not limit the diversity of a clam's developmental patterns. Possible explanations for this finding are discussed.     

Growth and reproduction in the Antarctic brooding bivalve Adacnarca nitens (Philobryidae) from the Ross Sea

We present information on the reproductive biology, population structure, and growth of the brooding Antarctic bivalve Adacnarca nitens Pelseneer 1903, from the Ross Sea, Antarctica. Individuals ranging from 0.85 to 6.00 mm were found attached to a hydrozoan colony. This species shows low fecundity and large egg size, common to other brooding species. The minimum size at which oogenesis was detected was 2.3 mm and the minimum size at which brooding was evident was 3.9 mm. Embryos of a full range of developmental stages were brooded simultaneously in females. The population showed a log–normal distribution and results suggest non-periodic reproduction with continuous embryonic development. The reproductive traits of A. nitens are discussed in the context of circum-Antarctic species distribution and limitations to dispersal in brooding benthic invertebrates.     

Biological and oceanographic insights from larval labrid (Pisces: Labridae) identification using mtDNA sequences

Polymerase chain reaction and direct comparison of mitochondrial DNA sequences from a cytochrome b gene fragment were used to identify two morphologically distinct larval types ofXyrichtys, a genus of tropical wrasse (Pisces: Labridae). Both larval types were collected during ichthyoplankton surveys on the Middle Atlantic Bight shelf in the summer of 1988. DNA sequence comparisons indicated that both types were larvae ofXyrichtys novacula (Linnaeus). Back-calculated birthdate distributions for those larvae collected on the Middle Atlantic Bight shelf demonstrated that the two larval types formed two distinct cohorts indicating a biological difference. The two distinct larval types may be a consequence of an ecophenotypic effect, or they may represent offspring from genetically distinct populations. These results emphasize that important biological and oceanographic information can be gained through the use of the polymerase chain reaction and DNA sequencing for larval identificaiton.     

Life-history variation in three coexisting cheilostome bryozoan species of the genus Stylopoma in Panamá

Life-history variation was studied in three sympatric species of Stylopoma Levinsen [S. spongites (Pallas), S. projecta Canu and Bassler and Stylopoma n. sp. 15] in Panamá. Bryozoan colonies were collected from 27 reefs along 300 km of the Caribbean coast of Panamá. The distribution and abundance of each species were very patchy, but with broad overlap in occurrence among localities and depths. Nevertheless, species differed considerably in colony size, size at first reproduction and numbers of brooding larvae; implying that interspecific differences in life-history traits may contribute to their coexistence. To examine closely this variation in life-history patterns, we grew, in a common garden experiment, the offspring of the two most common species that were obtained from parent colonies collected from several reefs. There were highly significant differences in growth rates and the timing and extent of sexual reproduction which corresponded well to patterns observed in individuals from the field. Other factors, including size of larvae, extent of secondary zooidal calcification and numbers of avicularia were also correlated with differences in life histories. Despite this additional complexity, however, ecological consequences of trade-offs in life history among modular species such as Stylopoma spp. appear very similar to those among unitary species.     

Low queen mating frequency in the seed-harvester ant Pogonomyrmex (Ephebomyrmex) pima: implications for the evolution of polyandry

The evolution of polyandry is a central problem in the study of insect mating systems, and both material and genetic benefits have been proposed to offset the presumed costs of multiple mating. Although most eusocial Hymenoptera queens mate with just one or occasionally two males, high levels of polyandry are exhibited by several taxa, including seed-harvester ants of the genus Pogonomyrmex. Previous studies of queen mating frequency in Pogonomyrmex have focused on monogynous (one queen per colony) species in the subgenus Pogonomyrmex. We performed a genetic mother–offspring analysis of mating frequency in Pogonomyrmex (Ephebomyrmex) pima, a queen-dimorphic species with dealate and intermorph queens that differ in colony structure (intermorph colonies contain multiple queens). Our results demonstrate that both dealate and intermorph queens of P. (E.) pima are typically single maters, unlike their congeners analyzed thus far. Polyandry appears to be a derived trait in Pogonomyrmex, but comparative tests between P. (E.) pima queen morphs and across the genus provide no evidence that it evolved as an adaptation to increase genetic diversity within colonies or to obtain more sperm, respectively.     

Pelagic larval development in the brooding Antarctic brachiopod Liothyrella uva

Larvae of the Antarctic brachiopod Liothyrella uva (Broderip, 1833) were released by brooding females between 10 and 15 January 1992. They were collected and cultured for the ensuing 45 d. At release they were at the gastrula stage, and were recognisable as the usual brachiopod three-lobed larva from around 18 d after release. At 22 d post-release, larvae began to congregate under shell fragments placed in culture vessels as potential settlement substrata. However, the larvae showed no signs of settlement which, combined with the absence of many of the attributes of mature larvae seen in previous studies, was taken as evidence that these larvae had not reached fully competent stages. Previous work had shown that L. uva spawns in October, indicating that the developmental period lasts for a minimum of between 115 and 160 d. The release and subsequent development of larvae also shows that what was previously thought to be a brooding species combines a long brooding period with a free-swimming phase. If this is true of other brachiopod species, then there may need to be a recategorization of some species from brooding to combined brooding and free-swimming developmental types. Even though the development period in L. uva was likely to have been underestimated because a fully competent stage was not reached, a comparison with development rates for temperate species indicated a slowing of between 8 and 70 times. This dramatic slowing of development rate in brachiopods now joins similar data previously reported for echinoderms and nemerteans, suggesting that this is a very widespred, perhaps universal, attribute of Antarctic marine invertebrates.     

Brooding behaviour and reproductive success in two species of free-living simultaneous hermaphrodites

Although polyclads are amongst the most structurally simple of the triploblastic metazoans, they adopt a wide range of reproductive strategies. Parental care behaviour in this group is yet to be quantified for any species. We assessed the significance of brooding behaviour to the reproductive success of two free-living marine flatworms. Echinoplana celerrima and Stylochus pygmaeus were collected from the field and placed in pairs in containers of filtered seawater where they laid batches of eggs. Both parents were then removed from half of the containers and the brooding behaviour and hatching success of eggs were quantified. There were interspecific differences in brooding behaviour. Egg masses were covered by one E. celerrima parent for 12 ± 2% of time, whereas egg masses of S. pygmaeus were covered by one or both parents simultaneously for 85 ± 8% of time. Egg batches were abandoned by both species immediately prior to the onset of hatching (10–12 days). Hatching success was generally high (~90%) and brooding did not enhance the hatching success of eggs. We assessed the significance of parental care to hatching success of E. celerrima egg masses in the presence of three potential egg predators; in the presence of other organisms. E. celerrima devoted less time to brooding; however, hatching success was not affected. The amount of time spent brooding eggs differed greatly between the two polyclad species but was not essential to their reproductive success under benign conditions. Parental care may be of adaptive value under more stressful environmental conditions commonly experienced in estuarine environments such as lowered salinity, increased hypoxia or turbidity. Covering egg batches may play an additional role of advertising sexual status and a willingness to care for eggs.     

Occurrence of inflated swimbladders in five species of lanternfishes (family Myctophidae) from waters off southern California

The swimbladders of three species of myctophid fishes (Symbolophorus californiensis, Tarletonbeania crenularis and Diaphus theta, collected in the Southern California Bight between 1963 and 1978), previously observed to have both inflated and noninflated swimbladders as adults, were examined to determine if the swimbladders either vary in their inflation on a diel basis or cease to be inflated and possibly become nonfunctional in some individuals. The swimbladders of two lanternfishes reported to lack inflated swimbladders as adults (Lampanyctus regalis and L. ritteri) were included in the study for comparison. Only the swimbladder of L. regalis did not increase in size with increasing fish size. In the remaining four species, both the lengths and volumes of noninflated swimbladders were positively correlated with fish standard length (SL). Although the swimbladder continued to increase in size, inflated swimbladders were not found in L. ritteri>2 mm SL. Inflated and noninflated swimbladders occurred in overlapping size ranges of S. californiensis, T. crenularis, and D. theta. Only 11% of the D. theta swimbladders were inflated, and the occurrence of inflated swimbladders dit not differ significantly with day vs night capture or fish size. Although the frequency of occurrence of inflated swimbladders decreased significantly in larger S. californiensis, both S. californiensis and T. crenularis caught at the surface at night with a neuston net had significantly higher proportions of inflated swimbladders than did those collected below the surface with either daytime or night-time trawls. The swimbladder does not appear to become nonfunctional in either species. Rather than maintaining either constant volumes or constant masses of gas in their swimbladders during their vertical migrations, both species may inflate their swimbladders only while in the surface waters at night, and have noninflated swimbladders while at other depths of their vertical ranges.     

Risk taking during parental care: a test of three hypotheses applied to the pied flycatcher

According to life-history theory, there will often be a conflict between investment in current versus future reproduction. If a predator appears during breeding, parents must make a compromise between ensuring the growth and survival of offspring (nest defence, feeding and brooding of young), and reducing the risk of predation to ensure their own survival. We model three hypotheses for the outcome of this conflict which are particularly relevant for altricial birds. They are not mutually exclusive, but focus on different costs and benefits. (1) Parental investment is determined by the parents’ own risk of predation. This hypothesis predicts that a lone parent should take smaller risks than a parent that has a mate. (2) Parental investment is related to the reproductive value of the offspring: Parents are predicted to take greater risks for larger broods, larger-sized or older offspring. (3) Finally, we present the new hypothesis that parental investment is related to the harm that offspring would suffer during a period of no parental care (incubation, brooding, feeding). This hypothesis predicts that parents should take greater risks for younger offspring, or for offspring in poorer condition, because the marginal benefit of parental care is largest in such cases. Hence, one may also expect that lone parents should take greater risks than two parents because their offspring are more in need of care. We tested these hypotheses on the pied flycatcher (Ficedula hypoleuca) by presenting a stuffed predator of the parents (a sparrowhawk, Accipiter nisus) close to the nest when parents were feeding the young. Risk taking was measured as the time that elapsed until the first visit to the nest. Most support was found for the ‘‘harm to offspring’’ hypothesis. Previous studies have usually measured the intensity of nest defence against typical nest predators, and have found evidence for the ‘‘reproductive value of offspring’’ hypothesis. However, our model predicts that the importance of the reproductive value of the offspring should decrease relative to the harm that offspring would suffer if they were not cared for when the predator type changes from a nest predator to a predator of adults, and when conditions for breeding turn from good to bad. Received: 13 April 1995/Accepted after revision: 11 March 1996     

Costs and benefits of communal rearing to female prairie voles (<Emphasis Type="Italic">Microtus ochrogaster</Emphasis>)

Communal rearing of offspring may help mothers maximize their investment in offspring at a reduced cost to their own bodily condition, thus maximizing their potential for reproductive success. The objective of this study was to quantify the costs and benefits of communal rearing to prairie vole (Microtus ochrogaster) pups and mothers. Mothers were assigned to one of three social units: solitary mothers, singularly breeding groups (i.e. one mother and one non-reproductive sister) and plurally breeding groups (i.e. two lactating sisters). For each type of social unit, some replicates were provided with food ad libitum, while others were provided with limited food. The body mass of focal mothers (i.e. the first mother to produce a litter) was a significant predictor of pup growth. Regardless of food availability, litters of focal mothers in plurally breeding groups gained more weight than litters reared by solitary mothers. Pups reared in singularly breeding groups were intermediate in weight gain, but did not gain significantly more weight than solitary offspring. There was no difference in the body mass of focal mothers from each type of social unit, regardless of food availability. Within plurally breeding groups, the weight gain of the two litters and body mass of focal and second mothers did not differ. However, focal mothers from plurally breeding groups nursed fewer pups than solitary mothers and also fewer pups than their nestmates when food was limited. Our results suggest that plural breeding results in greater fitness to mothers than solitary and singular breeding.Communicated by E. Korpimäki