Article

A New Case of Poecilogony From South America and the Implications of Nurse Eggs, Capsule Structure, and Maternal Brooding Behavior on the Development of Different Larval Types

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Abstract

Poecilogony is the production of different larval types within the same species. Although rare, poecilogonous species are ideal systems for testing the evolutionary and ecological implication of different developmental modes in marine invertebrates. Here, we described a new case of poecilogony, the Southern Hemisphere spionid Boccardia wellingtonensis. We used a combination of common-garden experiments, video recordings, and in vitro manipulations of individuals from three sites to (1) document the type of poecilogony, the brooding behavior of the mother, and the hatching process; (2) experimentally measure the effect of nurse eggs on the growth and type of larvae produced; and (3) document variation in the length of the brooding period, number of capsules, larvae, and nurse eggs of mothers from three sites to explore the potential for plasticity in reproductive traits. These results were compared to the previously reported poecilogonous species B. proboscidea, which resembles B. wellingtonensis in size, morphology, ecology, and reproductive strategy but differs in capsule structure. We found that in contrast to B. proboscidea, B. wellingtonensis produced larvae that, in isolation and in the presence of nurse eggs, developed into a wide range of offspring sizes. Mothers brood and hatch the larvae with frequent partial hatching of the brood during the brooding period. Although larvae could not liberate themselves, larvae crossed to other capsules as interconnections between capsules broke during the developmental period, potentially affecting food availability, sibling competition for nurse eggs, and cannibalism. Variation in brooding time and number of capsules deposited among sites suggest local adaptations. © 2015 Marine Biological Laboratory.

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... The poecilogonous polychaete B. wellingtonensis inhabits the intertidal zone of New Zealand, South Africa, and Chile. The females of this species have two types of reproduction: (1) Type I females produce only planktotrophic larvae and (2) Type III females produce planktotrophic larvae, nurse eggs, and adelphophagic larvae within the same capsule (Oyarzun and Brante, 2015). An important advantage of poecilogony is the absence of potential biases due to phylogenetic effects in interspecific analyses facilitating the study of life history traits. ...
... The general features of B. wellingtonensis are summarized in Table 1. To maintain cultures of the samples in the laboratory, we used methods previously described by Oyarzun and Brante (2015). For subsequent analyses, the samples were classified into Type I planktotrophic larvae (PLTI), Type III planktotrophic larvae (PLTIII), early adelphophagic larvae (EAL), late adelphophagic larvae (AL), and adults (A). ...
... Besides, the let-7 was down-regulated in planktotrophic larvae with respect to other larval types (PLTI: −3.19 and PLTIII: −4.3, p < .0001). Contrary to adelphophagic larvae of B. wellingtonensis, planktonic larvae arrest their development inside the ovicapsule because they do not have the ability to consume nurse eggs and use their energy to growth (Oyarzun and Brante, 2015). However, probably, these larvae are able to intake intracapsular fluid like nutritional source, as has been observed in other gastropods species (Brante et al., 2009). ...
Article
Poecilogony is a type of reproduction in which a species produces different types of larvae. Boccardia wellingtonensis, is a poecilogonous polychaete with females producing planktotrophic and adelphophagic larvae, in addition to nurse eggs, in the same capsule that differ in feeding behavior. It is still unclear why planktotrophs do not feed on nurse eggs during the intracapsular development and arrest its growth, while adelphophagic larvae consume nurse eggs and planktotrophic larvae inside the capsule, hatching as advance larvae or as juveniles. Here we characterized the expression of selected miRNAs from these two types of larvae and from adults in order to begin to understand the molecular mechanisms that regulate expression in this type of poecilogony. Results showed that adults and pre-hatching adelphophagic larvae have high levels of expression of miR-125, miR-87a and let-7, while adelphophages at early developmental stage had low levels of expression of miR-87b. Planktotrophic larvae showed low expression level of let-7. This work represents the first step in understanding the role of miRNAs in the development of different larval types in a poecilogonous species. We also propose to B. wellingtonensis as an interesting biological model to study the evolution of larval modes and reproductive strategies of marine invertebrates.
... For example, in the poecilogonous polychaetes Boccardia wellingtonensis and Boccardia proboscidea, females lay both planktotrophic and adelphophagic larvae in the same clutch or capsule. These larvae are morphologically similar but differ in their feeding capacities; while both larval types can swim and feed on plankton if they are released into the water, only adelphophagic larvae may feed on nurse eggs and other larvae inside the capsules 10,11 . This suggests the existence of underlying mechanisms, other than morphological traits, that would explain the feeding behavior and capacity of marine invertebrate larvae. ...
... Oyarzun and Brante 10 describe two reproductive strategies in this species: Type I females produce only planktotrophic larvae while Type III females produce capsules containing both planktotrophic and adelphophagic larvae, which are indistinguishable from one another in the early stages of development, as well as nurse eggs. While planktotrophic larvae stop growth at mid developmental stages and do not appear to feed inside their capsules, adelphophagic larvae feed on nurse eggs and other embryos until the offspring hatch at an advanced larval stage or as juveniles 10 (Supplementary File S5). Previous works have found differences in the enzymatic activity of some digestive enzymes, such as hydrolases, hydrolases acids, and glycosidase, in the larvae of B. wellingtonensis that could be associated with the different larval trophic modes observed in this species 13 . ...
... We observed more DEGs between PLTI and EAL than we did between PLTIII and EAL (Supplementary File S3A,B). In contrast to the congeneric species B. proboscidea, the Type III reproductive strategy in B. wellingtonensis is characterized by a wider range of larval sizes (PLTIII), which is probably influenced by intracapsular food availability 10 . This causes a high variance in the larval size, making it likely to find larvae in different developmental stages in the same capsule. ...
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The polychaete Boccardia wellingtonensis is a poecilogonous species that produces different larval types. Females may lay Type I capsules, in which only planktotrophic larvae are present, or Type III capsules that contain planktotrophic and adelphophagic larvae as well as nurse eggs. While planktotrophic larvae do not feed during encapsulation, adelphophagic larvae develop by feeding on nurse eggs and on other larvae inside the capsules and hatch at the juvenile stage. Previous works have not found differences in the morphology between the two larval types; thus, the factors explaining contrasting feeding abilities in larvae of this species are still unknown. In this paper, we use a transcriptomic approach to study the cellular and genetic mechanisms underlying the different larval trophic modes of B. wellingtonensis. By using approximately 624 million high-quality reads, we assemble the de novo transcriptome with 133,314 contigs, coding 32,390 putative proteins. We identify 5221 genes that are up-regulated in larval stages compared to their expression in adult individuals. The genetic expression profile differed between larval trophic modes, with genes involved in lipid metabolism and chaetogenesis over expressed in planktotrophic larvae. In contrast, up-regulated genes in adelphophagic larvae were associated with DNA replication and mRNA synthesis.
... Females may invest nutritious compounds directly in the egg, as lipids and/or protein in the yolk (lecithotrophy; that is, internal food reserves), or externally, as nurse eggs (ovophagy). This parental investment often promotes faster growth rates allowing the larvae to hatch in an advanced stage or in a shorter time (Chaparro, Lincoqueo, Schmidt, Veliz, & Pechenik, 2012;Cumplido, Pappalardo, Fernández, Averbuj, & Bigatti, 2011;Oyarzun & Brante, 2015;Radashevsky, 1994;Thomsen, Collin, & Carrillo-Baltodano, 2014). Low internal reserves or low female investment in intra-capsular food results in slow intracapsular developmental rates and premature hatching, forcing larvae to feed on plankton in the water column to complete their development (Guerao, Simeó, Anger, Urzúa, & Rotllant, 2012;Thorson, 1950). ...
... Nurse eggs originate as viable oocytes in the ovaries that experience vitellogenesis (either in the ovaries or freely in the coelom) but then undergo a programmed cell death to interrupt their regular development (Eckelbarger, 1984;Mackay & Gibson, 1999;Smith & Gibson, 1999). The production of nurse eggs and the larvae's ability to feed on them promote intra-capsular development to more advanced stages (Chaparro et al., 2012;Oyarzun & Brante, 2015). For example, in the gastropod Crepipatella dilatata (Lamarck, 1822), nurse eggs (mostly composed of proteins and lipids) provide additional resources to the ovophagic larvae (those feeding on nurse eggs), which can then hatch with a fivefold energy level compared to the larvae of C. peruviana, which lack nurse eggs (Chaparro et al., 2012). ...
... Poecilogony (i.e., a species having more than one type of larval development) is infrequent in nature and only found in polychaetes and gastropods. This type of reproduction results in broods containing offspring hatching either as planktonic larvae, as juvenile individuals, or as a combination of both (Krug, 2007;Krug, Gordon, & Romero, 2012;McDonald, Collin, & Lesoway, 2014;Oyarzun & Brante, 2015. These intra-specific differences are often related to the amount and source of energy provided by females for larval nutrition and the capacity of the larvae to use that nutritional source. ...
Article
The level of parental investment for larval nutrition may determine the life cycle in marine invertebrate species laying egg masses or capsules, where the food available for enclosed individuals would determine time and developmental stage of hatching. Most species show a unique type of larval development. However, few species are poecilogonous and combine more than one development type. Poecilogony, although scarcely studied, allows comparing different patterns of parental reproductive investment, without the phylogenetic effect of the species ancestral modes of development (phylogenetic inertia), to help to understand the factors determining life strategy evolution in marine invertebrates. The poecilogonous polychaete worm Boccardia wellingtonensis encapsulates and incubates its offspring, which then hatches as either planktotrophic larvae or benthic juveniles; while Boccardia chilensis shows a non‐poecilogonous reproductive type, producing only planktotrophic larvae. In this work, we estimated the bioenergetic and biochemical composition of brooding and non‐brooding females of B. wellingtonensis and B. chilensis to compare the costs of reproduction in these two species. Results showed that glucose, protein, lipid, and energy content were significantly higher in non‐brooding than in brooding females of B. wellingtonensis; but also contained significantly more glucose, protein, and lipid than females of B. chilensis (in absolute and relative dry weight values). The poecilogonous species showed higher energy content previous to laying offspring. Our results support the idea that the evolution of a certain reproductive and life history traits in marine invertebrates is related to adaptations in the female's reproductive investment.
... Gastrotrochs occur in irregular pattern. Modified chaetae develop in chaetiger V in late larvae (Söderström 1920, as Polydora natrix;Hartman 1941;Carrasco 1976;Woodwick 1977;Blake and Kudenov 1981;Duchêne 1984Duchêne , 1989Guérin 1991;Gibson 1997;Blake and Arnofsky 1999;Gibson and Smith 2004;Blake 2006;Kamel et al. 2010;Oyarzun and Brante 2015;Blake 2017). ...
... However, Sato-Okoshi (2000) reported that Japanese populations only show lecithotrophic development, with no (or a very short) planktonic stage after hatching. The larval morphology of this species agrees with the description of that of B. proboscidea documented in Hartman (1941), Woodwick (1977), Blake and Kudenov (1981), Gibson (1997), Gibson and Smith (2004), Kamel et al. (2010), and Oyarzun and Brante (2015). The dorsal pigment pattern of these larvae resembles that of the larvae of B. tricuspa (Hartman, 1939) described by Carrasco (1976, as B. proboscidea;fide Blake and Kudenov 1978), B. natrix (Söderström, 1920) described by Söderström (1920, as Polydora natrix), and B. columbiana Berkeley, 1927 described by Blake and Arnofsky (1999) and Blake (2006) in having a single row of mid-dorsal melanophores. ...
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Planktonic larvae of spionid polychaetes are among the most common and abundant group in coastal meroplankton worldwide. The present study reports the morphology of spionid larvae collected mainly from coastal waters of northeastern Japan that were identified by the comparison of adult and larval 18S and 16S rRNA gene sequences. The molecular analysis effectively discriminated the species. Adult sequences of 48 species from 14 genera ( Aonides Claparède, 1864; Boccardia Carazzi, 1893; Boccardiella Blake & Kudenov, 1978; Dipolydora Verrill, 1881; Laonice Malmgren, 1867; Malacoceros Quatrefages, 1843; Paraprionospio Caullery, 1914; Polydora Bosc, 1802; Prionospio Malmgren, 1867; Pseudopolydora Czerniavsky, 1881; Rhynchospio Hartman, 1936; Scolelepis Blainville, 1828; Spio Fabricius, 1785; Spiophanes Grube, 1860) and larval sequences of 41 species from 14 genera ( Aonides ; Boccardia ; Boccardiella ; Dipolydora ; Laonice ; Paraprionospio ; Poecilochaetus Claparède in Ehlers, 1875; Polydora ; Prionospio ; Pseudopolydora ; Rhynchospio ; Scolelepis ; Spio ; Spiophanes ) of spionid polychaetes were obtained; sequences of 27 of these species matched between adults and larvae. Morphology of the larvae was generally species‐specific, and larvae from the same genus mostly shared morphological features, with some exceptions. Color and number of eyes, overall body shape, and type and arrangement of pigmentation are the most obvious differences between genera or species. The morphological information on spionid larvae provided in this study contributes to species or genus level larval identification of this taxon in the studied area. Identification keys to genera and species of planktonic spionid larvae in northeastern Japan are provided. The preliminary results of the molecular phylogeny of the family Spionidae using 18S and 16S rRNA gene regions are also provided.
... Females of some species deposit extra-embryonic food sources within the capsules, which is consumed by the embryos during their encapsulated development (Rivest, 1983;Chaparro and Paschke, 1990;Ojeda and Chaparro, 2004;Chaparro et al., 2005Chaparro et al., , 2012. The presence of such nurse embryos or nurse eggs as an extra-embryonic energy source is especially common in polychaetes (Rasmussen, 1973;Oyarzun and Brante, 2015) and gastropods (Spight, 1976a;Gallardo, 1977Gallardo, , 1979aGallardo, , 1980Gallardo, , 1981Rivest, 1983;Pechenik et al., 1984;Segura et al., 2010;Smith and Thatje, 2013a). Nurse eggs can be ingested during a specific stage of intracapsular development (e.g. ...
Article
Encapsulated development with extraembryonic yolk may lead to competition for nutrients within egg capsules. In this research, different degrees of competition among embryos in subtidal egg capsules of Acanthina monodon resulted in considerable differences in hatching size. For newly hatched juveniles, individuals hatching from less crowded egg capsules showed better survival, larger SL, higher rates of oxygen consumption, and higher rates of food consumption. However, by 28 days after hatching, the largest surviving juveniles were the best-performing individuals, regardless of the initial embryo density within the capsules. In summary, more crowded egg capsules resulted in poorer survival. These findings may help to explain the variability seen in juvenile success in some field populations; much of that variation may reflect stressful experiences that the new recruits have had during the early stages of their encapsulated development.
... Only thirteen cases of poecilogony in marine organisms have been thoroughly studied and supported (seven spionid polychaetes [9,10], five sacoglossan gastropods [11] and one littorinimorph gastropod [12]). For molluscs, a total of 42 cases have been suggested [5,6], though only six cases are supported [11,12]. ...
Article
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Background: Poecilogony, the presence of two developmental modes in the same animal species, is a rare phenomenon. Few cases of poecilogony have been suggested for marine invertebrates including molluscs and even less stood extensive testing, mostly revealing a species pair with differing developmental modes. We studied a textbook example of poecilogony in the viviparous snail Planaxis sulcatus (Gastropoda: Planaxidae), for the first time throughout its entire distribution range. Results: In the Western Indian Ocean and Red Sea this intertidal species is observed to have large, shelled juveniles, whereas in the Indo-West Pacific planktotrophic veliger larvae are released from a subhaemocoelic brood pouch. We uncovered a shift in developmental modes across its range: from west to east successively earlier developmental stages are released. Furthermore, genetic data based on mitochondrial DNA suggests to recognize P. sulcatus as a single species rather than a group of cryptic species. A reconstruction of the ancestral area of P. sulcatus based on molecular data outlines the Western Indian Ocean and the Indo-West Pacific as area of origin. Conclusion: The findings supporting Planaxis sulcatus as a single widespread species and the geographical shift from one reproductive mode to another suggest for this species to truly represent a case of geographic poecilogony, i.e. differing developmental modes between populations of the same species. Furthermore, the results of our ancestral range estimation imply the release of planktotrophic larvae as the ancestral developmental mode.
... Although in some species, females produce egg capsules and then leave them alone, others brood their fertilized eggs until the embryos hatch, generating a close physical relationship between the mother and her offspring [5,6]. Although, through incubation, the capsules are physically protected by the mother [7][8][9], their multi-layered walls provide some extra levels of protection to the initial stages of development [2,[10][11][12][13]. ...
Article
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Among calyptraeid gastropods, males become females as they get older, and egg capsules containing developing embryos are maintained beneath the mother's shell until the encapsulated embryos hatch. Crepipatella dilatata is an interesting biological model considering that is an estuarine species and thus periodically exposed to elevated environment-physiological pressures. Presently, there is not much information about the reproductive biology and brooding parameters of this gastropod. This paper describes field and laboratory observations monitoring sex changes, brooding frequencies, sizes of brooding females, egg mass characteristics, and embryonic hatching conditions. Our findings indicate that C. dilatata is a direct-developing protandric hermaphrodite, changing from male to female when individuals were between 18 and 20 mm in shell length. At our study site in Quempillén estuary, females were found to be brooding almost continuously throughout the year, having an average maximum of 85% of simultaneous brooding, with a short rest from April through June. No relationship was found between the number of capsules per egg mass and the size of the brooding female. However, capsule size and the number of embryos and nurse eggs were strongly related to female size. The offspring hatched with an average shell length > 1 mm. About 25% of the hatched capsules were found to contain both metamorphosed (juveniles) and non-metamorphosed (veliger) individuals. The sizes of the latter were < 1000 μm. The length of hatching juveniles was inversely related to the number of individuals per capsule, which seems related to differences in the availability of nurse eggs per embryo. Although fecundity per reproductive event of this species is relatively low (maximum approx. 800 offspring per egg mass) compared with those of calyptraeid species showing mixed development, the overall reproductive potential of C. dilatata seems to be high considering that females can reproduce up to 5 times per year, protecting their encapsulated embryos from physical stresses until well-developed juveniles are released into the population, avoiding a dangerous pelagic period prior to metamorphosis.
... The developmental arrest of some encapsulated larvae that are well formed and the continued growth of others is known from disparate taxa but appears to be unusual in each clade. It is known from two species of spionid annelids (Oyarzun and Brante, 2015), one species of calyptraeid gastropod (McDonald et al., 2014), and the species of vermetid gastropod studied here. The spionids, calyptraeids, and vermetids are all taxa with great variety in the presence or absence of nurse eggs and in the ratio of nurse eggs to developing offspring. ...
Article
A small vermetid gastropod broods capsules containing nurse eggs and embryos that develop into small veligers. A few of these veligers continue development and growth while nurse eggs and developmentally arrested sibling veligers disappear. Survivors hatch as crawling pediveligers and juveniles. None of the veligers, if removed from capsules, swim in a directed way or withdraw into their shells, indicating that even the developing veligers are unsuited for extracapsular life until they can crawl. The shells of arrested veligers decalcify while their siblings grow. Few of the developmentally arrested veligers that were isolated from siblings and fed algal cells resumed detectable growth. Nurse eggs rather than cannibalism provide most of the food, but full growth of developing veligers depends on limited sharing; arrest of some siblings is a necessary adjunct of the nurse-egg feeding. Here, two developmental outcomes for larvae produced by developmental arrest of some (often termed poecilogony) serves instead as a means of brood reduction. Brood reduction is often attributed to family conflicts resulting from genetic differences. Another hypothesis is that a mother who cannot accurately sort numbers of nurse eggs and developing eggs into capsules could rely on brood reduction to adjust food for her offspring. At the extreme, an entirely random packaging would produce a binomial distribution of embryos in capsules, a very uneven distribution of food per embryo, and some capsules with no embryos. Males have yet to be found in this species, but even if reproduction is asexual, selection could still favor brood reduction.
... Universidad de Concepción ( Chile) Ecology and development of larval stages in marine invertebrates-A new case of poecilogony from South America and the implications of nurse eggs, capsule structure, and maternal brooding behavior on the development of different larval types ( Oyarzún and Brante, 2015)-The effects of nurse eggs and sibling interactions on the larval development of the poecilogonous annelid Boccardia proboscidea (Spionidae) ( Oyarzún and Brante, 2014) Plant evo-devo-Flower development and perianth identity candidate genes in the basal angiosperm Aristolochia fimbriata (Piperales: Aristolochiaceae) ( Pabón-Mora et al., 2015)-Analysis of the CYC/TB1 class of TCP transcription factors in basal angiosperms and magnoliids ( Horn et al., 2014) Paulino, Juliana Universidade de São Paulo ( Brazil) Floral morphology and development-Comparative development of rare cases of a polycarpellate gynoecium in an otherwise monocarpellate family, Leguminosae ( Paulino et al., 2014)-Floral developmental morphology of three Indigofera species (Leguminosae) and its systematic significance within Papilionoideae ( Paulino et al., 2011) Perez, Oscar * Pontificia Universidad Católica del Ecuador (Ecuador) ...
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Famous for its blind cavefish and Darwin's finches, Latin America is home to some of the richest biodiversity hotspots of our planet. The Latin American fauna and flora inspired and captivated naturalists from the nineteenth and twentieth centuries, including such notable pioneers such as Fritz Müller, Florentino Ameghino, and Léon Croizat who made a significant contribution to the study of embryology and evolutionary thinking. But, what are the historical and present contributions of the Latin American scientific community to Evo-Devo? Here, we provide the first comprehensive overview of the Evo-Devo laboratories based in Latin America and describe current lines of research based on endemic species, focusing on body plans and patterning, systematics, physiology, computational modeling approaches, ecology, and domestication. Literature searches reveal that Evo-Devo in Latin America is still in its early days; while showing encouraging indicators of productivity, it has not stabilized yet, because it relies on few and sparsely distributed laboratories. Coping with the rapid changes in national scientific policies and contributing to solve social and health issues specific to each region are among the main challenges faced by Latin American researchers. The 2015 inaugural meeting of the Pan-American Society for Evolutionary Developmental Biology played a pivotal role in bringing together Latin American researchers eager to initiate and consolidate regional and worldwide collaborative networks. Such networks will undoubtedly advance research on the extremely high genetic and phenotypic biodiversity of Latin America, bound to be an almost infinite source of amazement and fascinating findings for the Evo-Devo community.
... The developmental arrest of some encapsulated larvae that are well formed and the continued growth of others is known from disparate taxa but appears to be unusual in each clade. It is known from two species of spionid annelids (Oyarzun and Brante, 2015), one species of calyptraeid gastropod (McDonald et al., 2014), and the species of vermetid gastropod studied here. The spionids, calyptraeids, and vermetids are all taxa with great variety in the presence or absence of nurse eggs and in the ratio of nurse eggs to developing offspring. ...
... Moreover, how the adelphophagic behavior evolved in nemerteans, and which are-if any-the developmental changes associated with this event, is still unknown. Adelphophagy has been reported in several bilaterian groups, including vertebrates, echinoderms, insects, molluscs, annelids and platyhelminthes [89,90], and often involves heterochronic shifts in the maturation of feeding structures [91,92], changes in the morphology, composition and development of the nurturing-eggs [89,[93][94][95], and the development of specialized structures in the embryos [96][97][98]. Our study demonstrates that the ingestion of siblings in L. ruber starts before metamorphosis (Fig. 3), and extends during the whole time the post-metamorphic juveniles are inside the egg string. ...
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Background The life cycle of many animals includes a larval stage, which has diversified into an astonishing variety of ecological strategies. The Nemertea is a group of spiralians that exhibits a broad diversity of larval forms, including the iconic pilidium. A pelagic planktotrophic pilidium is the ancestral form in the Pilidiophora, but several lineages exhibit deviations of this condition, mostly as a transition to pelagic lecithotrophy. The most extreme case occurs, however, in the Pilidiophoran Lineus ruber, which exhibits an adelphophagic intracapsular pilidium, the so-called Schmidt’s larva. Results We combined confocal laser scanning microscopy and gene expression studies to characterize the development and metamorphosis of the Schmidt’s larva of L. ruber. The larva forms after gastrulation, and comprises a thin epidermis, a proboscis rudiment and two pairs of imaginal discs from which the juvenile will develop. The cells internalized during gastrulation form a blind gut and the blastopore gives rise to the mouth of the larva and juvenile. The Schmidt’s larva eats other siblings that occupy the same egg capsule, accumulating nutrients for the juvenile. A gradual metamorphosis involves the differentiation of the juvenile cell types from the imaginal discs and the shedding of the larval epidermis. The expression of evolutionarily conserved anterior (foxQ2, six3/6, gsc, otx), endomesodermal (foxA, GATA456-a, twi-a) and posterior (evx, cdx) markers demonstrate that the juvenile retains the molecular patterning of the Schmidt’s larva. After metamorphosis, the juveniles stay over 20 days within the egg masses, until they are fully mature and hatch. Conclusions The evolution of the intracapsular Schmidt’s larva involved the loss of the typical feeding structures of the planktotrophic pilidium and a precocious formation of the imaginal discs, as also observed in other pelagic lecithotrophic forms. However, no special adaptations are observed related to adelphophagy. As in planktotrophic pilidium, the molecular mechanism patterning the juvenile is only active in the imaginal discs and not during the early development of the larva, suggesting two separate molecular programs during nemertean embryogenesis. Our results illuminate the diversification of larval forms in the Pilidiophora and Nemertea, and thus on the developmental mechanisms underlying metazoan larval evolution.
... Moreover, how the adelphophagic behavior evolved in nemerteans, and which are-if any-the developmental changes associated with this event, is still unknown. Adelphophagy has been reported in several bilaterian groups, including vertebrates, echinoderms, insects, molluscs, annelids and platyhelminthes [89,90], and often involves heterochronic shifts in the maturation of feeding structures [91,92], changes in the morphology, composition and development of the nurturing-eggs [89,[93][94][95], and the development of specialized structures in the embryos [96][97][98]. Our study demonstrates that the ingestion of siblings in L. ruber starts before metamorphosis (Fig. 3), and extends during the whole time the post-metamorphic juveniles are inside the egg string. ...
Article
Full-text available
Background: The life cycle of many animals includes a larval stage, which has diversified into an astonishing variety of ecological strategies. The Nemertea is a group of spiralians that exhibits a broad diversity of larval forms, including the iconic pilidium. A pelagic planktotrophic pilidium is the ancestral form in the Pilidiophora, but several lineages exhibit deviations of this condition, mostly as a transition to pelagic lecithotrophy. The most extreme case occurs, however, in the Pilidiophoran Lineus ruber, which exhibits an adelphophagic intracapsular pilidium, the so-called Schmidt's larva. Results: We combined confocal laser scanning microscopy and gene expression studies to characterize the development and metamorphosis of the Schmidt's larva of L. ruber. The larva forms after gastrulation, and comprises a thin epidermis, a proboscis rudiment and two pairs of imaginal discs from which the juvenile will develop. The cells internalized during gastrulation form a blind gut and the blastopore gives rise to the mouth of the larva and juvenile. The Schmidt's larva eats other siblings that occupy the same egg capsule, accumulating nutrients for the juvenile. A gradual metamorphosis involves the differentiation of the juvenile cell types from the imaginal discs and the shedding of the larval epidermis. The expression of evolutionarily conserved anterior (foxQ2, six3/6, gsc, otx), endomesodermal (foxA, GATA456-a, twi-a) and posterior (evx, cdx) markers demonstrate that the juvenile retains the molecular patterning of the Schmidt's larva. After metamorphosis, the juveniles stay over 20 days within the egg masses, until they are fully mature and hatch. Conclusions: The evolution of the intracapsular Schmidt's larva involved the loss of the typical feeding structures of the planktotrophic pilidium and a precocious formation of the imaginal discs, as also observed in other pelagic lecithotrophic forms. However, no special adaptations are observed related to adelphophagy. As in planktotrophic pilidium, the molecular mechanism patterning the juvenile is only active in the imaginal discs and not during the early development of the larva, suggesting two separate molecular programs during nemertean embryogenesis. Our results illuminate the diversification of larval forms in the Pilidiophora and Nemertea, and thus on the developmental mechanisms underlying metazoan larval evolution.
Chapter
Investigating developmental evolution usually requires comparing differences across related species to infer how phenotypic change results from embryological modifications. However, when comparing organisms from different environments, ecologies, and evolutionary histories there can be many confounding factors to finding a genetic basis for developmental differences. In the marine annelid Streblospio benedicti, there are two distinct types of offspring with independent developmental pathways that converge on the same adult phenotype. To my knowledge, S. benedicti is the only known species that has heritable (additive) genetic variation in developmental traits that results in alternative life-history strategies. Females produce either hundreds of small, swimming and feeding larvae, or dozens of large, nonfeeding larvae. The larvae differ in their morphology, ecology, and dispersal potential. This developmental dimorphism makes S. benedicti a unique and useful model for understanding how genetic changes result in developmental modifications that ultimately lead to overall life-history differences. Because the offspring phenotypes of S. benedicti are heritable, we can use forward genetics within a single evolutionary lineage to disentangle how development evolves, and which genes and regulatory mechanisms are involved.
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Developmental mode describes the means by which larvae are provisioned with the nutrients they need to proceed through development, and typically results in a trade-off between offspring size and number. The sacoglossan sea slug Alderia willowi exhibits intraspecific variation for developmental mode (= poecilogony) that is environmentally modulated with populations producing more yolk-feeding (lecithotrophic) larvae during the summer, and more planktonic feeding (planktotrophic) larvae in the winter. I found significant family level variation in the reaction norms between 17 maternal families of A. willowi when reared in low (16 ppt) versus high (32 ppt) salinity. I documented a strong response to selection for lecithotrophic larvae, the proportion of which increased 32% after three generations of selection in high salinity, and 18% after 2 generations in low salinity (realized heritability: mean and SD, 0.365 and 0.024). The slope of the reaction norm was maintained following one generation of selection for lecithotrophy and one generation of selfing. The rapid response to selection favoring one developmental mode may speak to the rarity of intraspecific variation for developmental mode, which could fix for one mode over another much more readily than has generally been assumed from studies of less plastic organisms.
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In marine invertebrates, the modes of development at early stages are related to the type and capacity of larval feeding to achieve growth. Therefore, studying the factors that determine larval feeding strategies can help to understand the diversity of life histories and evolution of marine invertebrates. The polychaete Boccardia wellingtonensis is a poecilogonous species that encapsulates and incubates its offspring. This species produces two types of larvae: (1) larvae that do not feed within the capsule and hatch as planktotrophic larvae (indirect development), and (2) adelphophagic larvae that feed on nurse eggs and other larvae inside the capsule to hatch as advanced larvae or juveniles (direct development). Otherwise, the larval types are indistinguishable at the same stage of development. The non-apparent morphological differences between both types of larvae suggest that other factors are influencing their feeding behavior. This work studied the potential role of the activity of 19 digestive enzymes on the different feeding capacities of planktotrophic and adelphophagic larvae of B. wellingtonensis. Also, differences in larval feeding structures and the larval capacity to feed from intracapsular fluid were evaluated by electron and fluorescence microscopy. Results showed that both types of larvae present similar feeding structures and had the capacity to ingest intracapsular fluid protein. Adelphophagic larvae showed overall the highest activities of digestive enzymes. Significant differences between larval types were observed in nine enzymes related to the use of internal and external nutritional sources. Given that larval feeding is closely related to larval development in species with encapsulation, this work supports that the study of the digestive enzymatic machinery of larvae may contribute to understanding the evolution of developmental modes.
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For more than a century, evolutionary biologists, ecologists, and oceanographers alike have been intellectually stimulated by marine invertebrate larval forms. In 1995, Ecology of Marine Invertebrate Larvae, edited by the late Dr. Larry McEdward, captured the fundamental phenomenon and tremendous diversity of reproductive, biological, and oceanographic aspects of larval ecology. Now, more than twenty years later, this current edited volume provides an update to many of the original 13 chapters, while also reviewing several braches of larval ecology and evolution that have developed since. In Evolutionary Ecology of Marine Invertebrate Larvae, authors review the origins of marine invertebrate larvae and the developmental mechanisms and ecological factors that may generate this great diversity, and how these microscopic organisms feed, develop, and behave in the pelagic environment. Whether actively swimming in the coastal seas or the deep abyss, larvae are often in motion and must settle on the seafloor; however, if delayed, they are susceptible to certain consequences in subsequent stages later in life. Now, in an age of climate change, larvae face a warmer, more acidic, and more toxic ocean than ever before. Responses to these plus many other stressors and facets of larval biology can be broadly profiled, thanks to current technological advances. This edited volume provides a major synthesis of an important interdisciplinary field, as it aims to foster stimulating discussions centered on the evolution and ecology of marine invertebrate larvae. [https://global.oup.com/academic/product/evolutionary-ecology-of-marine-invertebrate-larvae-9780198786962?facet_narrowbyproducttype_facet=Digital&lang=en&cc=no]
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In this paper, the authors briefly review the reproduction and larval development of three poecilogonous species (Haminaea callidegenita, Streblospio benedicti and Capitella sp.) and pose the following questions: 1) Why are the currently known examples of poecilogonous species found only in polychaetes and opisthobranchs? 2) Why are poecilogonous animals predominately located on mud flats? 3) If poecilogony is such a good reproductive strategy, why don't we see it in more species? Polychaetes and opisthobranchs may be genetically predisposed for more flexible reproduction, and the mud flat is among the most dynamic marine habitat, exerting greater selective pressure favoring polymorphism of reproduction than that of other habitats.
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This paper examines the demographic consequences of planktotrophic and lecithotrophic development in an estuarine polychaete. Two strains of Streblospio benedicti (Spionidae) were reared in the laboratory from birth through death at 20⚬C and salinity 34 per mille. Survivorship and reproductive data were collected weekly and were used to construct life tables and population projection matrices for each development mode. Planktotrophic females reproduced earlier, and had higher fecundity and a shorter generation time than lecithotrophic females, but also exhibited higher mortality early in life. Despite the apparently opportunistic nature of the planktotrophic life history traits, the finite rate of increase (λ) in the lecithotrophic strain (1.319 wk-1) exceeded that of the planktotrophic strain (1.205 wk-1). Net reproductive rate (R0) was also higher for the lecithotrophs (93.4) than for the planktotrophs (17.6) Peak reproductive values were attained earlier in planktotrophs than in lecithotrophs. Sensitivity analyses indicate that λ is most sensitive to changes in larval and juvenile survivorship, and that the differences in λ were almost completely determined by life table differences during the first 15 wk of life. The potential population growth rates obtained in this study agree well with those estimated for other opportunistic polychaete species such as Capitella sp. I and Polydora ligni. Under uniform conditions the two strains of S. benedicti achieved similar growth rates with very different life history traits. We hypothesize that each combination of traits may be adaptive under different circumstances in the field.
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The reproduction, larval development and seasonal occurrence of planktonic larvae of eight species of Polydora from Maine are described. The species are: Polydora ligni, P. websteri, P. aggregata, P. commensalis, P. socialis, P. concharum, P. quadrilobata and P. caulleryi. The first seven named were reared from egg capsules and plankton isolates, while P. caulleryi larvae were only obtained from plankton isolates. A key to the polydorid larvae of New England is given.
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Adelphophagy, development where embryos grow large by consuming morphologically distinct nutritive embryos or their own normal siblings is widespread but uncommon among animal phyla. Among invertebrates it is particularly common in some families of marine gastropods and segmented worms, but rare or unknown in other closely related families. In calyptraeid gastropods phylogenetic analysis indicates that adelphophagy has arisen at least 9 times from species with planktotrophic larval development. This pattern of frequent parallel evolution of adelphophagy suggests that the embryos of planktotrophic species might be predisposed to evolve adelphophagy. Here we used embryos of three species of planktotrophic calyptraeids, one from each of three major genera in the family (Bostrycapulus, Crucibulum, and Crepidula), to answer the following 3 questions: (1) Can embryos of species with planktotrophic development benefit, in terms of pre-hatching growth, from the ingestion of yolk and tissue from experimentally damaged siblings? (2) Does ingestion of this material from damaged siblings increase variation in pre-hatching size? and (3) Does this experimentally induced adelphophagy alter the allometry between the velum and the shell, increasing morphological similarity to embryos of normally adelphophagic species? We found an overall increase in shell length and velum diameter when embryos feed on damaged siblings within their capsules. There was no detectable increase in variation in shell length or velum diameter, or changes in allometry. The overall effect of our treatment was small compared to the embryonic growth observed in naturally adelphophagic development. However each embryo in our experiment probably consumed less than one sibling on average, whereas natural adelphophages often each consume 10-30 or more siblings. These results suggest that the ability to consume, assimilate, and benefit from yolk and tissue of their siblings is widespread across calyptraeids.
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The role of dispersal potential on phylogeographic structure, evidenced by the degree of genetic structure and the presence of coincident genetic and biogeographic breaks, was evaluated in a macrogeographic comparative approach along the north-central coast of Chile, across the biogeographic transition zone at 30°S. Using 2,217 partial sequences of the mitochondrial Cytochrome Oxidase I gene of eight benthic invertebrate species along ca. 2,600 km of coast, we contrasted dispersal potential with genetic structure and determined the concordance between genetic divergence between biogeographic regions and the biogeographic transition zone at 30°S. Genetic diversity and differentiation highly differed between species with high and low dispersal potential. Dispersal potential, sometimes together with biogeographic region, was the factor that best explained the genetic structure of the eight species. The three low dispersal species, and one species assigned to the high dispersal category, had a phylogeographic discontinuity coincident with the biogeographic transition zone at 30°S. Furthermore, coalescent analyses based on the isolation-with-migration model validate that the split between biogeographic regions north and south of 30°S has a historic origin. The signatures of the historic break in high dispersers is parsimoniously explained by the homogenizing effects of gene flow that have erased the genetic signatures, if ever existed, in high dispersers. Of the four species with structure across the break, only two had significant albeit very low levels of asymmetric migration across the transition zone. Historic processes have led to the current biogeographic and phylogeographic structure of marine species with limited dispersal along the north-central coast of Chile, with a strong lasting impact in their genetic structure.
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Females of the polychaete Polydora hoplura (Claparède 1869) that produced planktotrophic and adelphophagic larvae were compared genetically to determine whether the different reproductive morphs represented sibling species or poecilogony. Worms were collected from Saldanha Bay, South Africa (33°0′37.71S, 17°56′59.74E), and cultured in a laboratory setting from November 2012 to April 2013. The results based on mitochondrial and nuclear DNA (Cyt b and ATPSα, respectively) showed shared haplotypes between reproductive morphs for both markers. Additionally, variation in mtDNA sequences was significantly higher within morphs than between morphs (95.8 and 4.2 %, respectively). A comparison of developmental modes found that broods of planktotrophic larvae were larger than broods of adelphophagic larvae, while the latter had larger eggs and larvae at hatching. Developmental time from oviposition to settlement for planktotrophic and adelphophagic larvae was 40.2 and 16.6 days, respectively. Polydora hoplura represents the fifth confirmed case of poecilogony in the Spionidae.
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Intracapsular development is common in marine gastropods. In many species, embryos develop alongside nurse eggs, which provide nutrition during ontogeny. The common whelk Buccinum undatum is a commercially important North Atlantic shallow-water gastropod. Development is intracapsular in this species, with individuals hatching as crawling juveniles. While its reproductive cycle has been well documented, further work is necessary to provide a complete description of encapsulated development. Here, using B. undatum egg masses from the south coast of England intracapsular development at 6 °C is described. Number of eggs, veligers and juveniles per capsule are compared, and nurse egg partitioning, timing of nurse egg consumption and intracapsular size differences through development are discussed. Total development took between 133 and 140 days, over which 7 ontogenetic stages were identified. The number of both eggs and veligers were significantly related to capsule volume, with approximately 1 % of eggs developing per capsule. Each early veliger consumed nurse eggs rapidly over just 3-7 days. Within each capsule, initial development was asynchronous, but it became synchronous during the veliger stage. No evidence for cannibalism was found during development, but large size differences between embryos developing within each capsule were observed, and occasionally `empty' veligers were seen, which had not successfully consumed any nurse eggs. These results indicate a high level of competition for nurse eggs within each capsule during development in the common whelk. The initial differences observed in nurse egg uptake may affect individual predisposition in later life.
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This study links offspring size and energetic content to offspring performance (measured as growth and survivorship) in the intertidal gastropod Nucella ostrina and examines the effect of hatching size on performance at different times of year and in contrasting environments. The relationships between individual hatchling size and organic content were compared both within and among clutches of N. ostrina. Hatchling size was positively, significantly, and predictively correlated with hatchling organic content both within and among clutches, demonstrating that hatching size could be reliably used as an indicator of maternal investment. The slope of the relationship between hatchling size and organic content varied between clutches, suggesting intrapopulation variation in embryonic growth geometry. In field outplants, hatching size always had a positive and significant effect on growth, and small hatchlings took approximately one month to reach the initial size of their larger siblings. More large hatchlings than small hatchlings were recovered in every experimental outplant. The: effect of hatching size on recovery was not significant in short (9 d) outplants, but recovery of large hatchlings was significantly greater than recovery of small hatchlings in two out of three long-term (36 or 54 d) outplants. Overall recovery was lower in the summer, the long-term outplant in which size did not significantly affect recovery. In experiments testing the relationship between hatching size and survivorship in two environments that differed in degree of sun exposure, size significantly and positively affected recovery in the more shaded habitat (with higher overall recovery) but not in the sun-exposed environment. Thus, larger hatching size in N. ostrina results in (1) increased hatchling growth, (2) considerably shortened time to maturity, and (3) higher survivorship. However, the advantage of large hatching size was decreased under more severe environmental conditions, those which resulted in higher overall hatchling mortality. Contrary to predictions, poor environmental conditions may not be more likely to select for large off spring size in intertidal habitats: during periods of high heat stress, mortality may be largely random with respect to size.
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Sibling cannibalism is commonly observed in marine species. For instance, intrabrood cannibalism has been documented in marine gastropods with direct development, suggesting a relationship between embryo behavior and the evolution of life history strategies. However, there has been little effort to document the factors driving sibling cannibalism in marine species. The kin selection theory suggests that the level of relatedness plays an important role in cannibalism patterns. We examined Crepidula coquimbensis, a marine gastropod that broods and encloses its brooded offspring in capsules. Encapsulated embryos show sibling cannibalism and high levels of intracapsular multiple paternity. Given these features, cannibalistic behavior may be driven by kin-relatedness. To test this hypothesis, we constructed artificial aggregations of embryos to mimic three levels of relatedness: high, medium and low. For each category of aggregation, the cannibalism rate and benefits (i.e. size at hatching of surviving offspring) were estimated. In addition, at the end of embryo development, we performed parentage analyses to determine if cannibalism was associated with the relatedness between cannibal and victim embryos. Our results show that the intensity of sibling cannibalism increased in aggregations characterized by the lowest level of relatedness. There were important benefits of cannibalism in terms of hatching cannibal size. In addition, cannibalism between embryos was not random: the variation in reproductive success between males increased over the course of the experiment and the effective number of fathers decreased. Altogether, these results suggest that polyandry may play an important role in the evolution of sibling cannibalism in C. coquimbensis and that kin selection may operate during early embryonic stages in this species.
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The larval development of Polydora giardi is described. Adults occur in burrows found in coralline algae and abalone shells. Sexes are separate. Females deposit eggs in hollow, cylindrical capsules attached to the wall of the tube by filaments. Larvae are released from capsules at the three-setiger stage. Planktonic development exceeds 25 days at 15° C. Larvae settle randomly on the surface of calcareous substrata and metamorphose in the presence of coralline algae. Only 8.3% of the population were sexually mature over a 6-month period from February through July. The larvae of P. giardi closely resemble those of P. flava, P. caeca, and P. concharum. This larval resemblance is also reflected in adult morphology.
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Many marine organisms are sedentary as adults and are redistributed between generations by the oceanic transport of planktonic larvae. In order to assess interactions among oceanographic and biological processes that determine larval dispersal patterns, we introduce a Lagrangian (or water-parcel-following) description of larval transport. This formalism is used to determine larval dispersal kernels (larval settlement probability distributions) for a range of ocean flows, planktonic larval durations and settlement pre-competency/competency periods. Paths of individual planktonic larval releases are modeled statistically and, by averaging over many individuals, ensemble estimates of larval dispersal are determined. Typical dispersal scales vary from a few km to >400 km. Modeled dispersal kernels are well explained using only a few readily available biological and oceanographic parameters, and derived dispersal scales agree well with population-genetic estimates, suggesting that the model has reasonable predictive power. An index for regional-scale self-seeding is presented, and is used as a tool to evaluate the efficiency of marine conservation areas. Finally, settlement patterns resulting from larval releases made over short times (days to months) should be comprised of a small number of discrete samples taken from the long-term averaged dispersal kernel. The resulting larval dispersal patterns will be quasi-random in both space and time, which will have important implications for the interpretation of settlement time series and the prediction of recruitment of sessile organisms.
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The spionid polychaete Pygospio elegans displays more than one developmental mode. Larvae may develop directly, ingesting nurse eggs while brooded in capsules within the parental tube, or they may hatch early to feed in the plankton before settling. Asexual reproduction by architomic fragmentation also occurs. Geographically separated populations of P, elegans often display different life histories. Such a variable life history within a single species may be interpreted either as evidence of sibling speciation or of reproductive flexibility (poecilogony). Four populations from the English Channel were found to demonstrate differing Life histories and were examined for morphological and genetic variability to determine whether P, elegams is in fact a cryptic species complex. Significant but minor inter-population polymorphisms were found in the distribution of branchiae and the extent of spoonlike hooded hooks. These externally polymorphic characters did not vary with relation to life history, and variation fell within the reported range for this species. Cellulose acetate electrophoresis was used to examine 10 allozyme loci, 5 of which were polymorphic. Overall, observed heterozygosity (H-o = 0.161) was lower than that expected under Hardy-Weinberg equilibrium (H-e = 0.228). Significant heterozygote deficiencies, detected at the Est* and Xdh* loci in all populations (except Xdh* at Ryde Sand, Isle of Wight, UK), are discussed. F-statistics were used to examine patterns of genetic structuring among both separate and pooled populations. F-ST values at all polymorphic loci indicated a significant level of genetic differentiation between populations, most probably related to isolation by geographic distance. No direct relationship between life history and genetic structure could be detected. Overall genetic identity among the 4 populations was high (I= 0.977 to 0.992). Overall, populations displaying larval brooding did not appear to be reproductively isolated from populations displaying a fully planktonic larval mode. Present data support the hypothesis that P. elegans is poecilogonous.
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Eight species of polydorid polychaetes were found to inhabit mollusc shells from south-western Australian waters. Numerous individuals of Polydora uncinata were extracted for the first time from the shells of both land-based cultured abalone Haliotis laevigata and H. roei, as well as from natural subtidal H. roei and Chlamys australis. Shells of the oyster Saccostrea commercialis cultured in sea-based systems were infested by Boccardia knoxi which was first recorded in these waters. Polydora aura, Dipolydora giardi, D. armata, D. aciculata and Boccardia proboscidea were common among shells of various natural intertidal and subtidal molluscs. A small number of P. haswelli were extracted from their self-excavated burrows in shells of cultured oysters. Boccardia knoxi and D. aciculata were redescribed based on the newly collected materials. Polydora uncinata and B. knoxi exhibited similar larval development patterns (exolecithotrophy and adelphophagy), iteroparity and longer life span, suggesting a high reproductive potential. This study suggests that further monitoring of polydorid species is needed not only from the viewpoint Of marine biology but also to survey the risk invasive species pose to commercially important molluscs in this region and worldwide.
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The oyster drill Urosalpinx cinerea deposits egg capsules containing eggs that are surrounded by a viscous albumen. The capsules do not contain nurse eggs, but during development the embryos appear to ingest the capsular albumen. In capsules collected from Long Island Sound, the number of embryos per capsule varied widely, as did capsule volume. Hatching size among these capsules also varied, and was strongly correlated with the mean volume of albumen available per embryo. The data suggest that in U. cinerea, albumen consumption by embryos increases their overall size at hatching and that differences among capsules in the volume of albumen available to the embryos result in a wide range of hatching sizes.
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The ability to produce more than one kind of offspring, or poecilogony, is a striking example of reproductive variability. Traditionally, larval nutrition has been classified as a dichotomy: if offspring obtain nutrition from their mothers (lecithotrophy), there is lower fecundity and greater chance of offspring survival than when they get their nutrition from plankton (planktotrophy). The polychaete Boccardia proboscidea (Spionidae) produces both types of embryos using three different reproductive strategies. In this study, we examined the roles of genetic history and phenotypic plasticity on explaining natural variation in B. proboscidea along the Pacific coast of the United States using two genetic mitochondrial markers, 16S rDNA and Cyt b, and common garden experiments. These data show a single North American West Coast network that is structured, geographically, by the well-documented biogeographic break near Point Conception, California. The southern group within this network covers a smaller range, but has larger haplotype diversity, than the northern group. Some individuals differing in reproductive type had the same haplotype, indicating independence of these features; however, differences between laboratory and field data suggest additional geographic variation within one of the reproductive types. Females from higher latitudes provide offspring with larger supplies of extra embryonic nutrition than females from southern latitudes. Results herein suggest that both genetic history and developmental plasticity are playing a role in the maintenance of this reproductive polymorphism.
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Development in marine invertebrate species can take place through a variety of modes and larval forms, but within a species, developmental mode is typically uniform. Poecilogony refers to the presence of more than one mode of development within a single species. True poecilogony is rare, however, and in some cases, apparent poecilogony is actually the result of variation in development mode among recently diverged cryptic species. We used a phylogenetic approach to examine whether poecilogony in the marine polychaete worm, Pygospio elegans, is the result of cryptic speciation. Populations of worms identified as P. elegansooded, and intermediate larvae; these modes are found both within and among populations. We examined sequence variation among partial mitochondrial cytochrome c oxidase subunit I sequences obtained for 279 individual worms sampled across broad geographic and environmental scales. Despite a large number of unique haplotypes (121 haplotypes from 279 individuals), sequence divergence among European samples was low (1.7%) with most of the sequence variation observed within populations, relative to the variation among regions. More importantly, we observed common haplotypes that were widespread among the populations we sampled, and the two most common haplotypes were shared between populations differing in developmental mode. Thus, our results support an earlier conclusion of poecilogony in P elegans. In addition, predominantly planktonic populations had a larger number of population-specific low-frequency haplotypes. This finding is largely consistent with interspecies comparisons showing high diversity for species with planktonic developmental modes in contrast to low diversity in species with brooded developmental modes.
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Cryptic species are increasingly recognized as commonplace among marine gastropods, especially in taxa such as shell-less opisthobranchs that lack many discrete taxonomic characters. Most cases of poe-cilogony, the presence of variable larval development within a single species, have historically turned out to represent cryptic species, with each possessing a single canalized type of development. One well-characterized example of poecilogony was attributed to the sacoglossan opisthobranch Alderia modesta; in southern California, slugs resembling this member of a monotypic genus produce both long-lived, planktotrophic and short-lived, lecithotrophic larvae. Paradoxically, however, A. modesta is exclusively planktotrophic everywhere else in the northern Pacific and Atlantic Oceans. A recently completed molecular study found that slugs from poecilogonous populations south of Bodega Harbor, California, comprise an evolutionarily distinct lineage separate from northern, strictly plank-totrophic slugs. We now describe the southern species as A. willowi n. sp., based on differences in mor-phology of the dorsum and radula, characteristics of the egg mass, larval development mode and nuclear and mitochondrial genetic markers. A DNA barcode is provided, based on 27 fixed differences in the cytochrome c oxidase subunit I gene that can reliably differentiate Pacific specimens of Alderia species. Genetic and morphological data are concordant with developmental evidence, confirming that A. willowi is a true case of poecilogony. An improved understanding of the ecological differences between these sister taxa may shed light on the selective pressures that drove the evolution of lecitho-trophy in the southern species.
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The reproduction and larval development of spioniform polychaetes are reviewed. Asexual reproduction is relatively rare, being reported for only eight species belonging to the genus Pygospio and some polydorids. Both architomy and paratomy are known, with the latter limited to small species of Pseudopolydora (sometimes referred to Polydorella) and one species of Polydora. Architomy is often the primary form of reproduction in Pygospio elegans and contributes to the maintenance of large populations. Three types of eggs (thin egg envelopes, thick egg envelopes, smooth or reticulated, and thick egg envelopes, honeycombed), two types of oogenesis (extraovarian and intraovarian), and two types of sperm (ect-aquasperm and introsperm) occur in spioniforms. Egg and sperm type are restricted to specific clades. Eggs with thickened egg envelopes appear to be limited to spioniforms, whereas the thin egg envelope found in some spionids occurs in other polychaete families, suggesting that thin egg envelopes are plesiomorphic for spionids. Spermatophores occur in the spionid subfamily Spioninae and are formed in the male nephridia. Spioniforms exhibit a diversity of reproductive and larval patterns including broadcast spawning, external egg masses, brooding in capsules in tubes of females and brooding on the bodies of females. Poecilogony is unusually common in the Spionidae. A phylogenetic analysis demonstrates that reproductive and larval characters, when used in combination with selected adult characters, provide a more complete database to evaluate systematic and phylogenetic relationships than only adult morphology. Preliminary results of parsimony suggest that the Spionidae are paraphyletic and that its definition and the status of related spioniform polychaetes needs to be reassessed with regard to family level classification.
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A Polydora species was found boring in shells of the abalone Haliotis discus hannai cultivated in land-based tanks in Coquimbo, Chile. Spionid polychaetes of Polydora and related genera have been reported from Chile but no worms similar to those found in abalone have been described. The abalone pest corresponds in morphology to Polydora uncinata Sato-Okoshi, 1998, a shell-boring species which was originally described from Japan and never reported from outside the country. It is suggested that occurrence of the species in Chile resulted from its accidental transportation from Japan. Adult worms were most likely transported to Coquimbo with imported abalone brood stock. Prevalence of abalone infestation by worms in Coquimbo varied substantially among cultivation tanks, reaching values as high as 98.8%. Up to 42 worms were found in one shell. The worms often caused formation of nacreous blisters which covered up to 50% of the inner shell surface. Egg capsules with developing larvae were present in female burrows. Larval development was entirely lecithotrophic, with larvae feeding on numerous nurse eggs, staying inside egg capsules until 16–17-segment stage and hatching shortly before metamorphosis. Polydora uncinata is redescribed based on individuals from Coquimbo to alert zoologists in case of accidental release of worms into Chilean coastal waters. Regardless of how the species was transported to Chile, its release to the natural ecosystem may have negative unforeseen impacts on the native fauna.
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Two new species of the subgenus Asteroporpa (Asteromoana) (Echinodermata: Ophiuroidea: Euryalida: Gorgonocephalidae) are described from southwestern and southern Japan. A. (Asterom.) muricatopatella sp. nov. has only cone-shaped dermal ossicles with terminal projections on radial shields, only plate-shaped dermal ossicles on oral plates, and coneshaped dermal ossicles with relatively short terminal projections at the lateral interradial disc. A. (Asterom.) koyoae sp. nov. has both cone-shaped dermal ossicles with terminal projections and plate-shaped dermal ossicles on radial shields, cone-shaped dermal ossicles with terminal projections on oral plates, and cone-shaped dermal ossicles with relatively long terminal projections on the lateral interradial disc. A taxonomic key to all four species of the subgenus A. (Asteromoana) is provided.
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Poecilogony is the production of more than one type of young within a single species of marine invertebrate. We chose a poecilogonous polychaete to investigate potential differences in morphogenesis among offspring that are polymorphic in dispersal potentials (planktonic, benthic) and trophic modes (planktotrophy, adelphophagy). Differences in morphogenesis occur and are strongly influenced by maternal type. Females that provide extra-embryonic nutrition (as nurse eggs; type III females) also produce offspring with an accelerated onset of juvenile traits, relative to planktotrophic offspring of females that do not provide extra-embryonic nutrition (type I females). Thus, progeny of some females appear morphologically preadapted for a benthic lifestyle. Surprisingly, differences in phenotype among offspring do not parallel offspring ecotype, as offspring with early onset of juvenile traits (III) are ecologically bimodal. Some Type III offspring eat the nurse eggs (adelphophagy), have accelerated development, and hatch as benthic juveniles. In contrast, their siblings hatch as small, planktotrophic, dispersive larvae that are morphologically similar to their type III siblings, but ecologically similar to Type I planktotrophic larvae. We propose that poecilogony evolved through sequence heterochrony in morphogenesis with accelerated onset of juvenile traits in type III offspring. In addition, we suggest that heterochrony in life-history events (hatching, metamorphosis) also occurs, thereby generating offspring that are dimorphic in both phenotype and ecotype. Over time, selection acting on different levels of ontogeny (morphogenesis vs. dispersal) may balance this polymorphism and allow poecilogony to persist.
Article
Invertebrate interspecific developmental patterns can be highly variable and, taxonomically, are considered only weakly constrained. Intraspecifically, some invertebrate species possess multiple developmental modes—a condition known as poecilogony. Closer examination of most putative poecilogenous species, however, has not supported poecilogony, but rather has uncovered hidden or cryptic species. The polychaete Streblospio benedicti is a well-known, poecilogenous species found along the coast of North America. We collected mitochondrial cytochrome subunit I DNA sequence data from 88 individuals taken from 11 locations along the Atlantic, Gulf, and Pacific Coasts of the United States to provide a phylogenetic framework from which to interpret intraspecific variation in larval life history and brooding structure morphology in this species. Our results are consistent with a recent revision of the species into two separate species: S. benedicti, a pouched brooding form distributed along the Atlantic and Pacific Coasts, and S. gynobranchiata, a branchiate brooding form in the Gulf of Mexico. Contrary to the redescription, S. benedicti is paraphyletic because the pouched brooding population in Vero Beach, Florida shows strong genetic affinity with Gulf of Mexico populations (S. gynobranchiata). However, S. benedicti is a true poecilogenous species, with both lecithotrophic and planktotrophic individuals possessing identical mitochondrial DNA haplotypes. Crossbreeding experiments further support the molecular phylogeny with reproductive isolation demonstrated between, but not within, the major phylogenetic clades consistent with the previously described species. The genetic break near Vero Beach, Florida, corresponds to a well-known phylogeographic boundary, but the estimated time of separation for the Streblospio spp., approximately 10 million years before present, predates all other known phylogeographic subdivisions in this area. This suggests that biogeographic sundering in this region is a recurrent event. Divergence times within the major Streblospio spp. clades are recent and indicate that changes in larval life history as well as brooding structure morphology are highly plastic and can evolve rapidly. Corresponding Editor: R. Burton
Article
A vermetid gastropod, previously unreported from the Pacific Ocean, was found at O‘ahu, Hawai‘i, in aquariums at the Kewalo Marine Laboratory, in fouling communities on docks, and on intertidal and shallow subtidal coral rubble. It also occurs on coral rubble in Florida. Eggs, or nurse eggs, and early embryos are about 100 μm in diameter. Young are brooded in 1–13 stalked capsules attached inside the tubular shell. Intracapsular development involves an unusual complex adelphophagy (sibling cannibalism). Most eggs are non-developing nurse eggs. Ten to 20 eggs develop into apparently normal small veligers. Of these most arrest as small veligers, but a few grow to hatch as large pediveligers or juveniles. The species has a high potential for invasion and establishment following maritime transport or natural rafting. Protected intracapsular development ends with the release of crawling hatchlings that also produce mucous threads on which they can drift. Juveniles settle readily on hard substrata. An apparent rarity or absence of males suggests long-term sperm storage, hermaphroditism, or parthenogenesis, any of which could aid colonization. Adults and juveniles occur in fouling communities and can survive extended periods in still seawater and at low food levels. The species' global distribution and history of invasions are unknown. We predict widespread distribution and invasions in warm waters.
Article
Compared 2 local demes (1.5km apart) of Streblospio benedicti (Spionidae). One was dominated by individuals exhibiting planktotrophy, where large numbers of offspring develop from small eggs as feeding larvae; the other was dominated by individuals exhibiting lecithotrophy, in which fewer numbers of larvae develop from large eggs without feeding. Over a 2.5yr period strong similarity was observed between demes in magnitude and timing of fluctuations in recruitment and total abundance, in benthic population size structure, and in secondary production, average production:biomass ratio, and annual population growth rates. Planktotrophs exhibited superior colonization ability, and showed greater seasonality and more variability in production and some demographic properties, suggesting that populations with planktotrophic development should exhibit different patch dynamics than those with lecithotrophic development. -Authors
Article
Boccardia proboscidea has poecilogonous development, i.e., it produces more than one type of offspring. Patterns of larval development within one population (La Jolla, CA) vary both among broods produced by different females, and also within a single brood, as some females produce both planktotrophic larvae and benthic juveniles within a single egg capsule. The mode of larval development is linked to the production of nurse eggs, non-viable eggs that are ingested by developing larvae (a process called adelphophagy). Not all females produce nurse eggs and most observed here produced only developing oocytes (Type 1 development). Type 1 females produce offspring that hatch at an early larval stage (3-setiger) and are planktotrophic for 30 d before metamorphosing. Type 2 females are similar to Type 1, but ~15% of the eggs per brood are non-developing nurse eggs. Type 2 offspring ingest the nurse eggs, larvae are slightly more advanced at hatching (3-5 setigers), and have a shorter planktotrophic period (19 d) than do Type 1 larvae. Type 3 females differ in that they produce broods in which most eggs (~90%) are nurse eggs. Offspring in Type 3 broods are either adelphophagic (ingest nurse eggs, have accelerated development, and hatch as juveniles) or non-adelphophagic (do not ingest nurse eggs and are similar to Type 1 planktotrophic larvae). Adults of each type are morphologically and ecologically similar and offspring of Type 1 and Type 3 females are interfertile. Although larval development varies among females, a single female will consistently produce broods of the same type. Poecilogony has been reported previously in B. proboscidea, but this is the first report of three developmental morphs within one population.
Article
Reproductive crosses between geographically separated populations of the nominal species, Polydora cornuta, support the hypothesis that the Florida/ Gulf of Mexico populations represent a single, potentially interbreeding lineage that is reproductively isolated from West Coast (California) and East Coast (Carolinas to Maine) populations. Previous research has indicated that California populations are reproductively compatible with worms from North Carolina but reproductively isolated from Maine populations. In spite of these species-level differences, all populations of this nominal species deposit egg capsules inside the female's tube that usually develop into three-chaetiger planktonic larvae measuring about 200 µm in length. Although adelphophagy (feeding upon unfertilized eggs within an egg capsule) has been reported in some populations of P. cornuta and in numerous other spionid polychaetes, the relationship between stored sperm in the female parent and the size of larvae within capsules has not been explored. We raised isolated female P. cornuta from three genetically and reproductively distinct populations (Florida, California and Maine) over a period of about 16 weeks and determined percent fertilization and larval size in successive spawnings over time until the females ran out of stored sperm. As each female used up stored sperm during successive spawnings, the percent of fertilized eggs per capsule declined and larval size at release increased. In some cases, the largest larvae produced by an isolated female were 114% larger than the smallest larvae produced by the same female. Larvae inside capsules containing unfertilized eggs fed upon these eggs and grew larger than larvae that did not have unfertilized eggs to feed upon. The effects of producing larger larvae following stored sperm depletion were completely reversed by transfer of fresh spermatophores to the isolated females. Variable larval size produced by a single female worm (poecilogony) may therefore be a result of stored sperm limitations rather than a genetically determined reproductive strategy in this species complex.
Article
In poecilogony, different types of larvae are produced within the same species. Previous studies have suggested maternal control of the production of larval types; however, it is not clear which factors or mechanisms generate contrasting developmental patterns among siblings. The spionid polychaete Boccardia proboscidea produces within the same capsule adelphophagic larvae that eat nurse eggs and siblings and complete all or most of their development inside the capsule (Type A larvae), and larvae with little growth until they hatch as planktotrophic larvae (Type B larvae). In this study, we manipulated capsule content to explore the factors determining larval type in B. proboscidea and the role of extra-embryonic maternal nutrition and sib–sib interaction in the developmental fate of offspring. When early larval stages were grown individually in vitro, with nurse eggs as the only food source, some of them remained small, while others continue developing into larger pre-competent larvae by feeding on nurse eggs. This suggests that larval types in B. proboscidea are determined very early in development and are not solely the product of sib–sib interaction inside the capsule. However, our data also suggest that hatching size variability within larval types of a clutch depends on nurse egg availability. Type B larvae grew normally to metamorphosis when phytoplankton was available, but suffered high rates of cannibalism by Type A larvae. These results are consistent with the hypothesis that individual larval fates are determined very early in development and that once their fate is determined, hatching size and intracapsular survival are affected by maternal food provisioning and sibling interaction.
Article
The concept of larval supply, and the relative importance of pre- and post-settlement processes as structuring agents of marine benthic invertebrate assemblages and communities are discussed. Because pelagic larvae result in an essential decoupling of local reproduction from local larval recruitment, many marine populations should be considered demographically ‘open’. Accordingly, factors affecting larval input to the benthos might be especially important in structuring both populations and communities, and even supercede the importance of post-settlement processes such as competition, predation and physical disturbance. Comprehensive studies on intertidal barnacles have provided an initial focus for field studies, but perhaps the greatest challenge facing marine ecologists lies in extrapolating beyond single-species populations to assess the relative importance of pre- and post-settlement processes for whole assemblages or communities.
Article
In marine invertebrates, polymorphism and polyphenism in mode of development are known as “poecilogony.” Understanding the environmental correlates of poecilogony and the developmental mechanisms that produce it could contribute to a better understanding of evolutionary transitions in mode of development. However, poecilogony is rare in marine invertebrates, with only ten recognized, well-documented cases. Five examples occur in sacoglossan gastropods, and five occur in spionid polychaetes. Here, we document the eleventh case, and the first in a caenogastropod mollusc. Females of Calyptraea lichen collected in the field or reared in the laboratory often produce broods of planktotrophic larvae. They can also be collected with mixed broods, in which each capsule contains planktotrophic larvae, nurse embryos, and adelphophagic embryos. Adelphophages eat the nurse embryos and hatch as short-lived lecithotrophic larvae, or even as juveniles. Mitochondrial COI and 16S DNA sequences for females with different types of broods differ by less than 0.5%, supporting conspecific status. Some females collected in the field with mixed broods subsequently produced planktotrophic broods, demonstrating that females can produce two different kinds of broods. Calyptraea lichen is therefore polyphenic in two ways: mode of development can vary among embryos within a capsule, and females can change the types of broods they produce.
Article
The concept of larval supply, and the relative importance of pre- and post-settlement processes as structuring agents of marine benthic invertebrate assemblages and communities are discussed. Because pelagic larvae result in an essential decoupling of local reproduction from local larval recruitment, many marine populations should be considered demographically ‘open’. Accordingly, factors affecting larval input to the benthos might be especially important in structuring both populations and communities, and even supercede the importance of post-settlement processes such as competition, predation and physical disturbance. Comprehensive studies on intertidal barnacles have provided an initial focus for field studies, but perhaps the greatest challenge facing marine ecologists lies in extrapolating beyond single-species populations to assess the relative importance of pre- and post-settlement processes for whole assemblages or communities. Amongst rocky intertidal assemblages, larval supply processes do appear especially important in circumstances where recruitment levels are low: at higher recruitment levels, post-settlement processes are prominent. No comprehensive evaluation of the relative importance of pre- and post-settlement processes has been undertaken for soft sediment assemblages, but the prevailing consensus is that hydrodynamic factors, density dependent effects of food availability and post-settlement processes are of prime importance. For epifaunal ‘fouling’ assemblages, probably both pre- and post-settlement factors are very important, and illustrative data are presented to show that post-recruitment processes may mask even strong larval signals in later assemblage development. Short-term panel data showed that hard substratum epifaunal recruitment levels do not necessarily conform to simple measures of current velocity at a given site: application of a tidal flushing model did, however, assist in explaining the variation in larval recruitment rates in relation to water flux below an arbitrary critical velocity for larval settlement. An indirect means of assessing realized larval dispersal – and hence geographic scale of population ‘openness’ – is available from analyses of population genetic differentiation. Data are presented for two species of epifaunal molluscs with contrasting larval types. The planktotrophic species conformed to expectations, in showing genetic homogeneity of populations over a 1600 km range, and therefore in displaying large-scale larval dispersal. The pelagic lecithotrophic species, however, revealed population differentiation on very small scales (< 10 km), even in highly dispersive environments with strong tidal currents (up to 3.6 m s-1). The deduction is that contrary to actually facilitating dispersal, those pelagic lecithotrophic larvae are behaviourally constrained to minimize larval transport. The consequences of this to general deductions about ‘openness’ of epifaunal assemblages are discussed, in the knowledge that spatial domination there is attributable largely to three phyla which characteristically reproduce by means of short-term pelagic lecithotrophic larval stages.
Article
The taxonomic, morphological, biological, behavioural and ecological characteristics of three species of spionid polychaetes from the Black Sea belonging to the Polydora-complex are summarised and discussed on the basis of the author′s collections along Romanian coasts as well as on material from other parts of the Black Sea. It is apparent that at least two species have been included under the name ′Polydora ciliata′ in the Black Sea literature. All previous records of Polydora that bore into calcareous substrates are most likely Polydora websteri. The individuals building muddy tubes on all types of substrata at depths less than 20 m, previously identified as P. ciliata or P. limicola, are P. cornuta. The presence of true P. ciliata in the Black Sea is questionable and older records must be re-evaluated. Dipolydora quadrilobata is a new record for the Romanian coast of the Black Sea, and has established dense populations in deeper (>30 m) soft bottom sediments. Descriptions and figures of these species, as well as a key to actual species of the Polydora-complex occurring in the Black Sea, are provided.
Article
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.
Article
In marine species, high dispersal is often associated with only mild genetic differentiation over large spatial scales. Despite this generalization, there are numerous reasons for the accumulation of genetic differences between,large, semi-isolated marine populations. A suite of well-known evolutionary mechanisms can operate within and between populations to result in genetic divergence, and these mechanisms may well be augmented by newly discovered genetic processes. This variety of mechanisms for genetic divergence is paralleled by great diversity in the types of reproductive isolation shown by recently diverged marine species. Differences in spawning time, mate recognition, environmental tolerance, and gamete compatibility have all been implicated in marine speciation events. There is substantial evidence for rapid evolution of reproductive isolation in strictly allopatric populations (e.g. across the Isthmus of Panama). Evidence for the action of selection in increasing reproductive isolation in sympatric populations is fragmentary. Although a great deal of information is available on population genetics, reproductive isolation, and cryptic or sibling species in marine environments, the influence of particular genetic changes on reproductive isolation is poorly understood for marine (or terrestrial) taxa. For a few systems, like the co-evolution of gamete recognition proteins, changes in a small number of genes may give rise to reproductive isolation. Such studies show how a focus on the physiology, ecology, or sensory biology of reproductive isolation can help uncover the genetic changes associated with speciation and can also help provide a link between the genetics of population divergence and the speciation process.
Article
A total of seven species of spionid polychaetes including one new species Dipolydora huelma were found from Puerto Montt and Chiloé Island (Chile). Polydora cf. rickettsi, Dipolydora huelma sp. nov. and D. giardi were extracted from self-excavated burrows in calcareous substrata: mollusc shells and coralline alga. Dipolydora socialis, Boccardia wellingtonensis, B. chilensis and B. tricuspa were found from mud, sand and sandstone intertidal flats. Boccardia wellingtonensis was re-examined, and Chilean specimens of B. polybranchia were re-examined and suggested that they may belong to B. wellingtonensis. Morphological variation, habitat, boring and crawling activity, ecology, reproduction and development, and burrow structure of each species is described and discussed.
Article
Planktonic marine invertebrate embryos and larvae lead transitory lives of great risk and grave uncertainty. Estimation of the magnitude of risk and mortality, however presents a formidable challenge. Three methods are currently in use to estimate levels of mortality among populations of marine invertebrate larvae: 1) theoretical models where rates of instantaneous mortality are correlated with other life history parameters, 2) estimation of mortality based on laboratory observations of predator-prey interactions and 3) analysis of relationships among gamete production, larval populations, and densities of post-larvae in the field. Theoretical exercises indicate that rates of larval mortality are correlated with duration of the planktonic period, and that differences in mortality rates may be offset by differences in egg size and fecundity. Results from laboratory investigations suggest that mortality rates change with larval size or age. Attempts to monitor cohorts of larvae in the plankton offer the most direct evidence for natural mortality, although they often lack confidence that larvae were sampled from a continuous population. Because factors that contribute to the mortality of marine invertebrate embryos and larvae operate concurrently and mortality is a density-dependent and age-specific demographic process, detailed investigations of several synergistic ecological parameters are required to provide meaningful estimates of instantaneous mortality rates in larval populations.
Article
Nurse eggs are commonly produced by spionid polychaetes and gastropod molluscs and serve as sources of extra-embryonic nutrition for developing young. Although the influence of nurse eggs on offspring development has been well documented, the origin of nurse eggs is not understood. We examined nurse egg production in the spionid Boccardia proboscidea using brightfield and fluorescence microscopy. Nurse eggs in this species appear to arise as do viable oocytes. After spawning, nurse eggs produce fertilization envelopes indicating that development has been activated. Nurse eggs are also capable of producing polar bodies, which indicates completion of meiosis in those eggs. After activation, nurse egg cytoplasm becomes compartmentalized into small bodies that are ingested by developing larvae and nuclear DNA is lost—processes similar to those observed in apoptotic cells. Thus, nurse egg production in B. proboscidea is an active developmental process and not simply an artifact of sperm limitation.
Article
In many species, alternative developmental pathways lead to the production of two distinct phenotypes, promoting the evolution of morphological novelty and diversification. Offspring type in marine invertebrates influences transport time by ocean currents, which dictate dispersal potential and gene flow, and thus has sweeping evolutionary effects on the potential for local adaptation and on rates of speciation, extinction and molecular evolution. Here, we use the polychaete Streblospio benedicti to investigate the effects of dimorphic offspring type on gene flow and genetic structure in coastal populations. We use 84 single nucleotide polymorphism (SNP) markers for this species to assay populations on the East and West Coasts of the United States. Using these markers, we found that in their native East Coast distribution, populations of S. benedicti have high-population genetic structure, but this structure is associated primarily with geographic separation rather than developmental differences. Interestingly, very little genetic differentiation is recovered between individuals of different development types when they occur in the same or nearby populations, further supporting that this is a true case of poecilogony. In addition, we were able to demonstrate that the recently introduced (~100 ya) West Coast populations probably originated from a lecithotrophic population near Delaware.
Article
Morphology is strongly correlated with trophic mode in marine invertebrate larvae. We asked if larval morphogenesis is influenced by adelphophagy, a trophic mode in which larvae are provisioned with additional yolk in the form of extra-embryonic nurse eggs, instead of the more common increase in egg size. We used histology and scanning electron microscopy to analyze morphogenesis in Boccardia proboscidea, a polychaete that produces both small planktotrophic larvae and large adelphophagic larvae in a single egg capsule. Results indicate that both morphs are similar for histogenesis of ectodermal derivatives, and differ for the gut mucosa and coelom which show delayed differentiation in the adelphophagic morph. Heterochrony in gut and coelom development suggests that differentiation of these organ systems is decoupled from overall development, and that a trade-off exists between maturation of these tissues and rapid growth. We also looked for potential barriers to adelphophagy in planktotrophic larvae that have nurse eggs available to them. These planktotrophic larvae appeared morphologically equipped for adelphophagy: the gut was differentiated at an early stage, and larvae had structures involved in nurse-egg ingestion in the adelphophagic morph (e.g., oral cilia and ventral ciliated patches). Planktotrophic larvae were additionally capable of ingesting particles (Di-I) while in the egg capsule. Lack of adelphophagy in planktotrophic larvae remains enigmatic but these results indicate that morphology alone does not account for the arrested development shown by these larvae. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.
Article
Trophic egg-laying – wherein mothers provide non-developing eggs for offspring to eat – has attracted much empirical attention to diverse taxa (e.g. amphibians, non-social and eusocial insects, fish, and marine gastropods). However, there has been been only a limited exchange of ideas among studies of different taxa. We advocate a unified approach to the study of trophic eggs within an evolutionary ecological framework. In this paper, we stress the importance of elucidating the adaptive function of trophic eggs through explicit hypothesis testing, and our primary objective is to outline key experiments that can test adaptive and functional hypotheses. Currently, some cases of hypothesized trophic eggs may simply represent offspring consumption of eggs that failed to develop for non-adaptive reasons (e.g. sperm limitation). Furthermore, in many trophic egg-laying species, it is unclear whether trophic eggs have evolved to provision offspring or to reduce cannibalism among offspring. With increased focus on theory and hypothesis testing, the study of trophic eggs can offer important insight into topics such as sibling rivalry, parent–offspring conflict, and parental care.
Article
In the marine gastropod Crepidula dilatata Lamarck, egg capsule height and width, the weight of the capsule wall, and the number of eggs per capsule increased with the female's shell length. However, since not all the eggs developed (some being nurse eggs), the number of embryos per capsule was independent of the shell length or dry tissue weight of the female parent, as were egg diameter and the number of capsules per brood. More than 90% of the energy invested in the egg mass was allocated to egg production, and less than 8% to constructing the capsules themselves. Small females produced embryos with a lower growth potential than that of embryos from larger females, because the larger the female, the more nurse eggs available to each embryo. The low energy investment in the production of capsule walls may be a consequence of `physical' parental care, because the female lays the capsules on the substratum and covers them with her shell throughout intracapsular development. The mean size of juveniles at hatching increased with the shell length of the female, because more nurse eggs were available to an embryo from a larger female than to an embryo from a smaller one. Larger juveniles may be at a competitive advantage in estuaries, where physical conditions vary over short time intervals and are often unfavourable.
Article
Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact support@jstor.org. Abstract. Studies in terrestrial systems suggest that long-distance propagule dispersal is important for landscape pattern and dynamics, but largely inconsequential for local demography. By contrast, in marine systems, dispersal at regional scales may drive local dynamics, because many species may have large mean dispersal distances. To assess var-iation in marine dispersal scales, we estimated mean dispersal distances from genetic iso-lation-by-distance slopes. Estimates ranged widely, from a few meters to hundreds of kilometers. Dispersal differed among taxonomic groups (macroalgae, invertebrates, and fish) and among species in different functional groups (e.g., producers and herbivores). Differences in dispersal scale have important implications for marine community dynamics, reserve design, responses to large-scale perturbations, and evolution of interacting species. To place genetic estimates of marine dispersal in context, we compared them to other measures of dispersal in the ocean and to estimates of dispersal on land. Maximum scales of dispersal by sedentary marine species exceeded maximum estimates of terrestrial plant dispersal by at least one to two orders of magnitude. Direct and genetic estimates of terrestrial plant dispersal were comparable to estimates of marine plant dispersal. Rates of marine macroalgal range expansion, however, far exceeded spread rates of terrestrial plants. Terrestrial plant spread rates were more similar to those of short-dispersing marine organ-isms that lack secondary dispersal by drifting adults. Genetic estimates of dispersal by different functional groups suggest that herbivores typically disperse much farther than their plant resources both on land and in the sea, although the timing, frequency, and consequences of dispersal may differ in the two systems. Terrestrial herbivores have more flexible dispersal behavior than marine organisms that disperse each generation by plank-tonic transport of larvae. Our results validate some long-standing views about the greater dispersal potential of species in the ocean, but also highlight the extreme heterogeneity in dispersal scale among marine species. As a result, development of a community perspective on marine connectivity will require consideration of multiple dispersal mechanisms and scales.
Article
Summary1. In analysing the ecological conditions of an animal population we have above all to focus our attention upon the most sensitive stages within the life cycle of the animal, that is, the period of breeding and larval development.2. Most animal populations on the sea bottom maintain the qualitatively composition of the species composing them, over long periods of time, though the individual species use quite different modes of reproduction and development. This shows that species producing a large number of eggs have a larger wastage of eggs and larvae than those with only a few eggs. The wastage of eggs in the sea is much larger than on the land and in fresh water.3. In the invertebrate populations on the level sea bottom, large fluctuations in numbers from year to year indicate species with a long pelagic larval life, while a more or less constant occurrence indicates species with a very short pelagic life or a non-pelagic development.4. In most marine invertebrates which shed their eggs and sperm freely in the water, either (a) the males are the first to spawn, thus stimulating the females to shed their eggs, or (b) an ‘epidemic spawning’ of a whole population takes place within a few hours. Both methods greatly favour the possibility of fertilization of the eggs spawned and show that the heavy wastage of eggs and larvae takes place after fertilization, during the free swimming pelagic life.5. Embryos with a non-pelagic development may originate (a) from large yolky eggs, in which case all the hatching young of the same species will be at the same stage of development, or (b) from small eggs which during their development feed on nurse eggs, when the individual embryos of the same species may vary enormously in size at the stage of hatching.6. Three types of pelagic larvae are known: (a) Lecithotrophic larvae, originating from large yolky eggs spawned in small numbers by the individual mother animals; they are independent of the plankton as a source of food although growing during pelagic life, are absent from high arctic seas but constitute about 1o% of the species with pelagic larvae in all other seas, (b) The planktotrophic larvae with a long pelagic life, originating from small eggs spawned in huge numbers by the individual mother animal; they feed from, and grow in, the plankton, constituting less than 5% of high arctic bottom invertebrates, 55–65% of the species in boreal seas, and 8o-85 % of the tropical species, (c) The planktotrophic larvae with a short pelagic life having the same size and organization at the moment of hatching and at the moment of settling; these constitute about 5% of the species in all Recent seas.7. To find out the factors which cause the enormous waste of eggs and larvae, we thus have to study those forms (constituting 7o% of all species of bottom invertebrates in Recent seas) which have a long planktotrophic pelagic life, as only species reproducing in this way have really large numbers of eggs.8. The food requirements of the planktotrophic pelagic larvae are much greater than those of the adult animals at the bottom. The adaptability of the larvae to poor food conditions seems, nevertheless, to be greater than hitherto believed. The significance of starvation seems mainly to be an indirect one: poor food conditions cause slow growth, prolong larval life, and give the enemies a longer interval of time to attack and eat the larvae.9. At the temperatures to which they are normally exposed, northern as well as tropical larvae seem on an average to spend a similar time (about 3 weeks) in the plankton. The length of the pelagic life of the individual species may, however, vary significantly in nature. In the Sound (Denmark) the larvae are never exposed to temperatures outside the range which they are able to endure. The wastage caused by temperature, like that due to starvation, seems mainly to be an indirect one: low temperatures postpone growth and metamorphosis, and give the enemies a longer time to feed on the larvae.1o. When a larva feeding on a pure algal diet metamorphoses into a carnivorous bottom stage, a ‘physiological revolution’ occurs and a huge waste of larvae might be expected. Experiments have, however, shown that this is not the case.11. Young pelagic larvae are photopositive and crowd near the surface; larvae about to metamorphose are photonegative. Larval polychaetes, echinoderms, and presumably also prosobranchs, may prolong their pelagic life for days or weeks until they find a suitable substratum. Forced towards the bottom by their photonegativity and transported by currents over wide bottom areas, testing the substratum at intervals, their chance of finding a suitable place for settling is much better than hitherto believed.12. Continuous currents from the continental shelf towards the open ocean may transport larvae from the coast to the deep sea where they will perish. Such conditions may (for instance in the Gulf of Guinea) deeply influence the composition of the fauna, while in other areas (European western coast, southern California) they seem to be only of small significance.13. The toll levied by enemies appears to be the most essential source of waste among the larvae. A list of such enemies, comprising other pelagic larvae, holoplank-tonic animals and bottom animals, is given on p. 2o. A medium-sized Mytilus edulis, filtering 1–4 1. of water per hour, may retain and kill about 100,000 pelagic lamellibranch larvae in 24 hr. during the maximum breeding season in a Danish fjord.14. Species reproducing in a vegetative way, by fission, laceration, budding, etc., might be expected to have good chances of competition in such areas where conditions for sexual reproduction are unfavourable. Nevertheless, they only supply a rather small percentage of the animal populations of all Recent seas, probably because their intensity of reproduction is low and because they are unable to spread to new areas. Most forms reproducing in a vegetative way have sexual reproduction as well.15. Pelagic development is nearly or totally suspended in the deep sea, and is restricted to the shelf faunas. In the arctic and antarctic seas pelagic development is nearly or totally suppressed, even in the shelf faunas, but starting from here the percentage of forms with pelagic larvae gradually increases as we pass into warmer water, reaching its summit on the tropic shelves.16. In order to survive in high arctic areas a planktotrophic, pelagic larva has to complete its development from hatching to metamorphosis within I–I ½ months (i.e. the period during which phytoplankton production takes place) at a temperature below 2–4o C. Most larvae, that is in 95% of the species, are unable to do so and have a non-pelagic development, but if a pelagic larva is able to develop under these severe conditions the planktotrophic pelagic life seems to afford good opportunities even in the Arctic. Thus the 5 % of arctic invertebrates reproducing in this way comprise several of the species which quantitatively are most common within the area.17. The antarctic shore fauna has poor conditions similar to those of the Arctic. The longest continuous periods of phytoplankton production are 2 and 3 weeks respectively, and pelagic larvae have, in order to survive, to complete their development within this short space of time at a temperature between 1 and 4o C. Accordingly, non-pelagic development is the rule, but most arctic species are able to support their non-pelagic development by means of much smaller eggs than the antarctic species, where brood protection and viviparity is dominant. The antarctic fauna has apparently had a longer time to develop its tendency to abandon a pelagic life. The greater the size of the individual born, the smaller its relative food requirements and the better its chance of competing under poor food conditions.18. The relatively few data on reproduction in deep sea invertebrates point to a non-pelagic development. The larvae of such forms, in order to develop through a planktotrophic pelagic stage, would have to rise by the aid of their own locomotory organs through a water column 2000–4000 m. high or more (often with counteracting currents) to the food producing surface layer, and to cover the same distance when descending to metamorphose and settle.19. The ecological features common to the deep sea, the arctic and the antarctic seas, which enable the same animals to live and to reproduce there, contribute to explain the ‘equatorial submergence’ of many arctic and antarctic coastal forms.20. In the tropical coastal zones where the percentage of species with pelagic larvae reaches its maximum, the production of food for the larvae takes place much more continuously than in temperate and arctic seas, because light conditions enable the phytoplankton to assimilate all the year round. The tropical species of marine invertebrates breed (in contrast to temperate and arctic species) within such different seasons that their larval stock, taken as a whole, is more or less equally distributed in the plankton all the year round. This makes the competition in the plankton less keen.21. The fact that a mode of reproduction and development, well fit for an arctic area, is unfit in a temperate or tropical area of the sea is probably one of the main reasons for the restricted distribution of species.22. In most groups of marine invertebrates the individual species have only one mode of reproduction and development, which accordingly restricts their area of distribution. In the polychaetes, however, the individual species often show an astonishing lability in their mode of reproduction and development which enables them to compete in wide areas of the sea. Thus, out of the Western European species of polychaetes, 28-4% have been found also in the Indian Ocean, and 18%, at least, along the Californian coast, while the corresponding number of Western European echinoderms, prosobranchs and lamellibranchs found also in the Indian Ocean and California amounts to less than 2%.23. The pelagic or non-pelagic development of marine prosobranchs has proved to be a very fine ‘barometer’ for ecological conditions. Recent observations, still not elaborated, seem to indicate that the shape of the top whorls, the apex, of the adult shells of prosobranchs may show whether the species in question has a pelagic or a non-pelagic development. This discovery may also give us valuable information about the larval development in fossil species, and help us to form an idea about ecological conditions in sea areas from earlier geological periods.
Article
A San Diego population of the opisthobranch mollusc Alderia modesta (Lovén, 1844) exhibits poecilogony, the presence of two development modes within a single species. In spring, half of the adults spawned masses containing ∼300 eggs with a mean diameter of 68 μm. After 3 d, these egg masses hatched planktotrophic veligers with a maximum shell dimension of 116 μm. The remaining adults spawned masses containing ∼30 eggs with a mean diameter of 105 μm. These egg masses hatched after 5 to 6 d, releasing lecithotrophic larvae with a maximum shell dimension of 186 μm. About 1% of field-collected adults produced mixed clutches containing a continuum of larval sizes, spanning the size extremes of planktotrophy and lecithotrophy and hatching larvae with a mean maximum shell dimension of 152 μm. Adults producing planktotrophic and lecithotrophic larvae were interfertile, and no hybrid breakdown was observed through the F3 generation. When starved, adults which previously produced only lecithotrophic larvae switched to producing planktotrophic larvae or mixed clutches with both planktotrophic and lecithotrophic larvae. Sequence-polymorphisms from a portion of the mitochondrial cytochrome c oxidase I gene support the conclusion that the two reproductive morphs represent a single species. Most of the lecithotrophic larvae and a small percentage of the larvae from mixed clutches were metamorphically competent within 3 d of hatching. A. modesta is the only molluscan species as yet known to have both planktotrophic and pelagic lecithotrophic development within a single natural population.
Article
Most species of benthic marine invertebrates have a single mode of larval development. Poecilogonous species are those that produce more than one type of larval offspring. Reports of variable development within one species, especially in combination with widely differing ecological habitat, are frequently attributed to cryptic species. The spionid polychaete Boccardia proboscidea Hartman, 1940 exhibits development that varies both within a single brood and among broods produced by different females. Some females have planktotrophic development and produce many small larvae with a 2 week planktonic period before metamorphosis. Other females produce broods containing both planktotrophic larvae as well as nurse-egg-ingesting (adelphophagic) offspring that hatch as juveniles. Molecular analysis (RAPD-PCR) showed that a significant proportion of genetic variance is attributable to geographic origin, and not to developmental type. Adults of both developmental types showed no consistent differences in taxonomically important features (e.g. type and arrangement of chaetae, modified fifth setiger, caruncle, branchiae, pygidium) when examined with SEM. These data support the hypothesis that developmental variability in this species is a case of poecilogony, and is not attributable to cryptic species.
Article
Credible cases of poecilogony, the production of two distinct larval morphs within a species, are extremely rare in marine invertebrates, yet peculiarly common in a clade of herbivorous sea slugs, the Sacoglossa. Only five animal species have been reported to express dimorphic egg sizes that result in planktotrophic and lecithotrophic larvae: the spionid polychaete Streblospio benedicti and four sacoglossans distributed in temperate estuaries or the Caribbean. Here, we present developmental and genetic evidence for a fifth case of poecilogony via egg-size dimorphism in the Sacoglossa and the first example from the tropical Indo-Pacific. The sea slug Elysia pusilla produced both planktotrophic and lecithotrophic larvae in Guam and Japan. Levels of genetic divergence within populations were markedly low and rule out cryptic species. However, divergence among populations was exceptionally high (10-12% at the mitochondrial cytochrome c oxidase I locus), illustrating that extensive phylogeographic structure can persist in spite of the dispersal potential of planktotrophic larvae. We review reproductive, developmental, and ecological data for the five known cases of poecilogony in the Sacoglossa, including new data for Costasiella ocellifera from the Caribbean. We hypothesize that sacoglossans achieve lecithotrophy at smaller egg sizes than do related clades of marine heterobranchs, which may facilitate developmental plasticity that is otherwise vanishingly rare among animals. Insight into the environmental drivers and evolutionary results of shifts in larval type will continue to be gleaned from population-level studies of poecilogonous taxa like E. pusilla, and should inform life-history theory about the causes and consequences of alternative development modes in marine animals.