Distinguishing Between Embryonic Provisioning Strategies in Teleost Fishes Using a Threshold Value for Parentotrophy.

The source of embryonic nutrition for development varies across teleost fishes. A parentotrophy index (ratio of neonate: ovulated egg dry mass) is often used to determine provisioning strategy, but the methodologies used vary across studies. The variation in source and preservation of tissue, staging of embryos, and estimation approach impedes our ability to discern between methodological and biological differences in parentotrophy indices inter- and intra-specifically. The threshold value used to distinguish between lecithotrophy and parentotrophy (0.6-1) differs considerably across studies. The lack of a standardised approach in definition and application of parentotrophy indices has contributed to inconsistent classifications of provisioning strategy. Consistency in both methodology used to obtain a parentotrophy index, and in the classification of provisioning strategy using a threshold value are essential to reliably distinguish between provisioning strategies in teleosts. We discuss alternative methods for determining parentotrophy and suggest consistent standards for obtaining and interpreting parentotrophy indices.

Placentation in the Mexican scincid lizard Plestiodon brevirostris (Squamata: Scincidae).

Viviparity is the reproductive pattern in which females gestate eggs within their reproductive tract to complete their development and give birth to live offspring. Within extant sauropsids, only the Squamata (e.g., snakes, lizards, and amphisbaenians) evolved viviparity, representing 20% of the existing species. The genus Plestiodon is represented by 43 species and is one of the most widely distributed genera of the Scincidae in Mexico. The goal of this research has been to determine the placental morphology and ontogeny during gestation in the lizard Plestiodon brevirostris. Specimens were dissected to obtain the embryonic chambers and the embryos were categorized to carry out the correlation between the development stage and the placenta development. The embryonic chambers were processed using the conventional histological technique for light microscopy. The identified embryonic stages were 4, 29, 34, 36, and 39. A thin eggshell surrounds the egg in early developmental stages; however, this structure is already absent in the embryonic hemisphere during the developmental stage 29. The results revealed that P. brevirostris is a lecithotrophic species, but a close maternal-fetal relationship is established by tissue apposition. Ontogenically, the placental types that form in the embryonic hemisphere are the chorioplacenta, choriovitelline placenta, and chorioallantoic placenta; whereas the omphaloplacenta is formed in the abembryonic hemisphere. The structure of the chorioallantoic placenta in P. brevirostris suggests that it may play a role during gas exchange between the mother and the embryo, due to the characteristics of the epithelia that comprise it. The structure of embryonic and maternal epithelia of the omphaloplacenta suggests a role in the absorption of the eggshell during gestation and possibly in the transport or diffusion of some nutrients. In general, it is evident that ontogeny and placental characteristics of P. brevirostris match those of other species of viviparous lecithotrophic scincids.

Increased superfetation precedes the evolution of advanced degrees of placentotrophy in viviparous fishes of the family Poeciliidae.

The causes and consequences of the evolution of placentotrophy (post-fertilization nutrition of developing embryos of viviparous organisms by means of a maternal placenta) in non-mammalian vertebrates are still not fully understood. In particular, in the fish family Poeciliidae there is an evolutionary link between placentotrophy and superfetation (ability of females to simultaneously bear embryos at distinct developmental stages), with no conclusive evidence for which of these two traits facilitates the evolution of more advanced degrees of the other. Using a robust phylogenetic comparative method based on Ornstein-Uhlenbeck models of adaptive evolution and data from 36 poeciliid species, we detected a clear causality pattern. The evolution of extensive placentotrophy has been facilitated by the preceding evolution of more simultaneous broods. Therefore, placentas became increasingly complex as an adaptive response to evolutionary increases in the degree of superfetation. This finding represents a substantial contribution to our knowledge of the factors that have shaped placental evolution in poeciliid fishes.

Plasticity and artificial selection for developmental mode in a poecilogonous sea slug.

The contribution of phenotypically plastic traits to evolution depends on the degree of environmental influence on the target of selection (the phenotype) as well as the underlying genetic structure of the trait and plastic response. Likewise, maternal effects can help or hinder evolution through affects to the response to selection. 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 a split-brood design in low (16 ppt) versus high (32 ppt) salinity, conditions which mimic seasonal variation in salinity of natural populations. I documented a significant response to selection for lecithotrophic larvae in high and low salinity. The slope of the reaction norm was maintained following one generation of selection for lecithotrophy. When the maternal environment was controlled in the laboratory, I found significant maternal effects, which reduced the response to selection. These results suggest there is standing genetic variation for egg-mass type in A. willowi, but the ability of selection to act on that variation may depend on the environment in which the phenotype is expressed in preceding generations.

Female reproductive mode shapes allometric scaling of male traits in live-bearing fishes (family Poeciliidae).

Reproductive mode is predicted to influence the form of sexual selection. The viviparity-driven conflict hypothesis posits that a shift from lecithotrophic (yolk-nourished) to matrotrophic (mother-nourished or placental) viviparity drives a shift from precopulatory towards post-copulatory sexual selection. In lecithotrophic species, we predict that precopulatory sexual selection will manifest as males exhibiting a broad distribution of sizes, and small and large males exhibiting contrasting phenotypes (morphology and coloration); conversely, in matrotrophic species, an emphasis on post-copulatory sexual selection will preclude these patterns. We test these predictions by gathering data on male size, morphology and coloration for five sympatric Costa Rican poeciliid species that differ in reproductive mode (i.e. lecithotrophy vs. matrotrophy). We find tentative support for these predictions of the viviparity-driven conflict hypothesis, with some interesting caveats and subtleties. In particular, we find that the three lecithotrophic species tend to show a broader distribution of male sizes than matrotrophic species. Furthermore, large males of such species tend to exhibit proportionately large dorsal and caudal fins and short gonopodia relative to small males, while these patterns are expressed to a lesser extent in the two matrotrophic species. Finally, large males in some of the lecithotrophic species exhibit darker fins relative to small males, a pattern not evident in either matrotrophic species. One unexpected finding was that even in the matrotrophic species Poeciliopsis retropinna and Poeciliopsis paucimaculata, which lack courtship and dichromatic coloration, some morphological traits exhibit significant allometric relationships, suggesting that even in these species precopulatory sexual selection may be present and shaping size-specific male phenotypes in subtle ways.

Viviparity in the longest-living vertebrate, the Greenland shark (Somniosus microcephalus).

BACKGROUND: The Greenland shark is renowned for its great longevity, yet little is known about its reproduction. METHODS: We supplemented the sparse information on this species by extrapolation from observations on other members of the sleeper shark family and the order Squaliformes. RESULTS AND CONCLUSION: The Greenland shark is viviparous and a single observation suggests a litter size of about ten. The gestation period is unknown, but embryos reach a length of around 40 cm at birth. Nutrition is derived from the yolk sac with minimal histotrophy. The surface area of the uterus is increased by villi that presumably increase in length with advancing gestation. These villi are not likely to be secretory but play a key role in the oxygen supply to the embryo. We argue that the ability of the uterus to supply oxygen is a limiting factor for litter size, which is not likely to exceed the small number reported in this and other sleeper sharks.

Structural changes to the uterus of the dwarf ornate wobbegong shark (Orectolobus ornatus) during pregnancy.

Embryos of the viviparous dwarf ornate wobbegong shark (Orectolobus ornatus) develop without a placenta, unattached to the uterine wall of their mother. Here, we present the first light microscopy study of the uterus of O. ornatus throughout pregnancy. At the beginning of pregnancy, the uterine luminal epithelium and underlying connective tissue become folded to form uterine ridges. By mid to late pregnancy, the luminal surface is extensively folded and long luminal uterine villi are abundant. Compared to the nonpregnant uterus, uterine vasculature is increased during pregnancy. Additionally, as pregnancy progresses the uterine epithelium is attenuated so that there is minimal uterine tissue separating large maternal blood vessels from the fluid that surrounds developing embryos. We conclude that the uterus of O. ornatus undergoes an extensive morphological transformation during pregnancy. These uterine modifications likely support developing embryos via embryonic respiratory gas exchange, waste removal, water balance, and mineral transfer.

Larval Performance of Amphidromous and Landlocked Atyid Shrimp Species in the Genus Paratya under Different Feeding Conditions.

Freshwater shrimps in the family Atyidae exhibit two life history traits: 1) amphidromy, with many small embryos hatching into planktotrophic larvae that develop in the sea, and 2) landlocked, with few large embryos hatching into non-feeding lecithotrophic larvae, or facultative lecithotrophic larvae that develop in freshwater. The lecithotrophy of larvae is considered an adaptation to limited food conditions in the freshwater environment. Furthermore, faster development and settlement behaviours that large larvae exhibit are considered adaptations that allow the larvae to stay in or near parental habitats in fast-flowing streams. We therefore hypothesized that the facultative lecithotrophic larvae of landlocked shrimps might better adapt to limited food conditions as their large body size develops, an adaptation to maintain habitat position in flowing streams, than do planktotrophic larvae of companion amphidromous species developing in the sea. To test this hypothesis, we compared the larval feeding habits and size of two closely related species in the genus Paratya: the amphidromous P. compressa, with planktotrophic larvae, and the landlocked P. improvisa, with facultative lecithotrophic larvae. Larvae were reared by being fed commercially preserved or cultured phytoplankton (Tetraselmis sp.) and cultured zooplankton rotifers. Paratya compressa larvae did not survive, but P. improvisa larvae did develop into the juvenile stage under poor feeding conditions with preserved Tetraselmis alone, supporting our hypothesis of the effects of different larval feeding habits in amphidromous and landlocked atyid shrimp species. Hatchlings were larger and larval duration was shorter in P. improvisa than in P. compressa. Paratya improvisa larvae exhibited settlement behaviour beginning with the early zoeal stage. Our results also highlighted the retention strategy by which landlocked P. improvisa larvae stay in or near parental habitats.

The secret life of deep-sea shrimps: ecological and evolutionary clues from the larval description of Systellaspis debilis (Caridea: Oplophoridae).

Currently there are 21 shrimp species in the northeastern Atlantic and Mediterranean Sea which are considered to belong to the superfamily Oplophoroidea, but the larval development is unknown for most of them. The complete larval development of Systellaspis debilis (Milne-Edwards, 1881), here described and illustrated, is the first one to have been successfully reared in the laboratory, consisting of four zoeal and one decapodid stages. The zoeae were found to be fully lecithotrophic, which together with the females' lower fecundity, are probably evolutionary consequences of the species mesopelagic habitat.

Culturing echinoderm larvae through metamorphosis.

Echinoderms are favored study organisms not only in cell and developmental biology, but also physiology, larval biology, benthic ecology, population biology and paleontology, among other fields. However, many echinoderm embryology labs are not well-equipped to continue to rear the post-embryonic stages that result. This is unfortunate, as such labs are thus unable to address many intriguing biological phenomena, related to their own cell and developmental biology studies, that emerge during larval and juvenile stages. To facilitate broader studies of post-embryonic echinoderms, we provide here our collective experience rearing these organisms, with suggestions to try and pitfalls to avoid. Furthermore, we present information on rearing larvae from small laboratory to large aquaculture scales. Finally, we review taxon-specific approaches to larval rearing through metamorphosis in each of the four most commonly-studied echinoderm classes-asteroids, echinoids, holothuroids and ophiuroids.

Mechanisms of reproductive allocation as drivers of developmental plasticity in reptiles.

Developmental plasticity in offspring phenotype occurs as a result of the environmental conditions embryos experience during development. The nutritional environment provided to a fetus is an important source of developmental plasticity. Reptiles are a particularly interesting system to study this plasticity because of their varied routes of maternal nutrient allocation to reproduction. Most reptiles provide their offspring with all or most of the nutrients they require in egg yolk (lecithotrophy) while viviparous reptiles also provide their offspring with nutrients via a placenta (placentotrophy). We review the ways in which both lecithotrophy and placentotrophy can lead to differences in the nutrients embryonic reptiles receive, and discuss how these differences lead to developmental plasticity in offspring phenotype. We finish by reviewing the ecological and conservation consequences of nutritional-driven developmental plasticity in reptiles. If nutritional-driven developmental plasticity has fitness consequences, then understanding the basis of this plasticity has exciting potential to identify how reptile recruitment is affected by environmental changes in food supply. Such knowledge is critical to our ability to protect taxa threatened by environmental change.

Do larval types affect genetic connectivity at sea? Testing hypothesis in two sibling marine gastropods with contrasting larval development.

In marine environments, connectivity among populations of benthic invertebrates is provided primarily by dispersion of larvae, with the duration of pelagic larval phase (PLD) supposed to represent one of the major factor affecting connectivity. In marine gastropods, PLD is linked to specific larval development types, which may be entirely intracapsular (thus lacking a pelagic dispersal), or include a short pelagic lecithotrophic or a long planktotrophic phase. In the present study, we investigated two sibling species of the cosmopolitan neogastropod genus Columbella (commonly known as dove shells): Columbella adansoni Menke, 1853, from the Macaronesian Atlantic archipelagos, with planktotrophic development, and Columbella rustica Linnaeus, 1758, from the Mediterranean Sea, with intracapsular development. We expected to find differences between these two sister species, in terms of phylogeographic structure, levels of genetic diversification and spatial distribution of genetic diversity, if PLD was actually a relevant factor affecting connectivity. By analysing the sequence variation at the cytochrome c oxidase subunit I (COI) in 167 specimens of the two species, collected over a comparable geographic range, we found that Columbella adansoni, the species with planktotrophic development, and thus longer PLD, showed no phylogeographic structure, lower levels of genetic diversity, interpopulational variance lower than the intrapopulational one and no spatial structure in the distribution of the genetic diversity; Columbella rustica, the species with intracapsular development, thus with evidently lower dispersal abilities, showed a clear phylogeographic structure, higher levels of genetic diversity, high interpopulational and low intrapopulational variance, and a clear signature of global spatial structure in the distribution of the genetic diversity. Thus, in this study, two sibling species differing almost only in their larval ecology (and PLD), when compared for their genetic variation showed patterns supporting the hypothesis that PLD is a major factor affecting genetic connectivity. Therefore, it seems reasonable to expect that the ecological attributes of the marine communities - also in terms of the variation in larval ecology of the species involved - are taken into the due consideration in conservation actions, like the design of marine protected areas networks.

Development of a lecithotrophic pilidium larva illustrates convergent evolution of trochophore-like morphology.

BACKGROUND: The pilidium larva is an idiosyncrasy defining one clade of marine invertebrates, the Pilidiophora (Nemertea, Spiralia). Uniquely, in pilidial development, the juvenile worm forms from a series of isolated rudiments called imaginal discs, then erupts through and devours the larval body during catastrophic metamorphosis. A typical pilidium is planktotrophic and looks like a hat with earflaps, but pilidial diversity is much broader and includes several types of non-feeding pilidia. One of the most intriguing recently discovered types is the lecithotrophic pilidium nielseni of an undescribed species, Micrura sp. "dark" (Lineidae, Heteronemertea, Pilidiophora). The egg-shaped pilidium nielseni bears two transverse circumferential ciliary bands evoking the prototroch and telotroch of the trochophore larva found in some other spiralian phyla (e.g. annelids), but undergoes catastrophic metamorphosis similar to that of other pilidia. While it is clear that the resemblance to the trochophore is convergent, it is not clear how pilidium nielseni acquired this striking morphological similarity. RESULTS: Here, using light and confocal microscopy, we describe the development of pilidium nielseni from fertilization to metamorphosis, and demonstrate that fundamental aspects of pilidial development are conserved. The juvenile forms via three pairs of imaginal discs and two unpaired rudiments inside a distinct larval epidermis, which is devoured by the juvenile during rapid metamorphosis. Pilidium nielseni even develops transient, reduced lobes and lappets in early stages, re-creating the hat-like appearance of a typical pilidium. Notably, its two transverse ciliary bands can be ontogenetically linked to the primary ciliary band spanning the larval lobes and lappets of the typical planktotrophic pilidium. CONCLUSIONS: Our data shows that the development of pilidium nielseni differs remarkably from that of the trochophore, even though their larval morphology is superficially similar. Pilidium nielseni's morphological and developmental features are best explained by transition from planktotrophy to lecithotrophy in the context of pilidial development, rather than by retention of or reversal to what is often assumed to be the spiralian ancestral larval type - the trochophore. Development of pilidium nielseni is a compelling example of convergent evolution of a trochophore-like body plan within Spiralia.

Patterns and Drivers of Egg Pigment Intensity and Colour Diversity in the Ocean: A Meta-Analysis of Phylum Echinodermata.

Egg pigmentation is proposed to serve numerous ecological, physiological, and adaptive functions in egg-laying animals. Despite the predominance and taxonomic diversity of egg layers, syntheses reviewing the putative functions and drivers of egg pigmentation have been relatively narrow in scope, centring almost exclusively on birds. Nonvertebrate and aquatic species are essentially overlooked, yet many of them produce maternally provisioned eggs in strikingly varied colours, from pale yellow to bright red or green. We explore the ways in which these colour patterns correlate with behavioural, morphological, geographic and phylogenetic variables in extant classes of Echinodermata, a phylum that has close phylogenetic ties with chordates and representatives in nearly all marine environments. Results of multivariate analyses show that intensely pigmented eggs are characteristic of pelagic or external development whereas pale eggs are commonly brooded internally. Of the five egg colours catalogued, orange and yellow are the most common. Yellow eggs are a primitive character, associated with all types of development (predominant in internal brooders), whereas green eggs are always pelagic, occur in the most derived orders of each class and are restricted to the Indo-Pacific Ocean. Orange eggs are geographically ubiquitous and may represent a 'universal' egg pigment that functions well under a diversity of environmental conditions. Finally, green occurs chiefly in the classes Holothuroidea and Ophiuroidea, orange in Asteroidea, yellow in Echinoidea, and brown in Holothuroidea. By examining an unprecedented combination of egg colours/intensities and reproductive strategies, this phylum-wide study sheds new light on the role and drivers of egg pigmentation, drawing parallels with theories developed from the study of more derived vertebrate taxa. The primary use of pigments (of any colour) to protect externally developing eggs from oxidative damage and predation is supported by the comparatively pale colour of equally large, internally brooded eggs. Secondarily, geographic location drives the evolution of egg colour diversity, presumably through the selection of better-adapted, more costly pigments in response to ecological pressure.

Reproductive cycle and maternal-embryonic nutritional relationship of shovelnose guitarfish Pseudobatos productus in the Gulf of California.

Samples of the shovelnose guitarfish Pseudobatos productus were collected on board a vessel and at landings of artisanal commercial fisheries in the Gulf of California from May 2004 to June 2007. Samples of 650 females, 2047 embryos and 484 uterine eggs were examined. The reproductive cycle is annual, ovulation and parturition occur in July, the uterine eggs are in diapause for 9 months (July-March) before an accelerated growth of embryos of 3 months. Histological analyses of the uterine wall of pregnant females suggested that no secretions were used for embryo nourishment. The standard percentage of water content was 48·6% in fertilized eggs and 80·75% in full-term embryos. Dry mass loss during embryonic development was 16·3% and the chemical balance of development was 0·84. This indicates that P. productus is a strictly lecithotrophic, viviparous species, that makes no maternal contribution of nutrients during embryonic development.

Reduced genetic diversity and increased reproductive isolation follow population-level loss of larval dispersal in a marine gastropod.

Population-level consequences of dispersal ability remain poorly understood, especially for marine animals in which dispersal is typically considered a species-level trait governed by oceanographic transport of microscopic larvae. Transitions from dispersive (planktotrophic) to nondispersive, aplanktonic larvae are predicted to reduce connectivity, genetic diversity within populations, and the spatial scale at which reproductive isolation evolves. However, larval dimorphism within a species is rare, precluding population-level tests. We show the sea slug Costasiella ocellifera expresses both larval morphs in Florida and the Caribbean, regions with divergent mitochondrial lineages. Planktotrophy predominated at 11 sites, 10 of which formed a highly connected and genetically diverse Caribbean metapopulation. Four populations expressed mainly aplanktonic development and had markedly reduced connectivity, and lower genetic diversity at one mitochondrial and six nuclear loci. Aplanktonic dams showed partial postzygotic isolation in most interpopulation crosses, regardless of genetic or geographic distance to the sire's source, suggesting that outbreeding depression affects fragmented populations. Dams from genetically isolated and neighboring populations also exhibited premating isolation, consistent with reinforcement contingent on historical interaction. By increasing self-recruitment and genetic drift, the loss of dispersal may thus initiate a feedback loop resulting in the evolution of reproductive isolation over small spatial scales in the sea.

Have superfetation and matrotrophy facilitated the evolution of larger offspring in poeciliid fishes?

Superfetation is the ability of females to simultaneously carry multiple broods of embryos, with each brood at a different developmental stage. Matrotrophy is the post-fertilization maternal provisioning of nutrients to developing embryos throughout gestation. Several studies have demonstrated that, in viviparous fishes, superfetation and matrotrophy have evolved in a correlated way, such that species capable of bearing several simultaneous broods also exhibit advanced degrees of post-fertilization provisioning. The adaptive value of the concurrent presence of both reproductive modes may be associated with the production of larger newborns, which in turn may result in enhanced offspring fitness. In this study, we tested two hypotheses: (1) species with superfetation and moderate or extensive matrotrophy give birth to larger offspring compared to species without superfetation or matrotrophy; (2) species with higher degrees of superfetation and matrotrophy (i.e. more simultaneous broods and increased amounts of post-fertilization provisioning) give birth to larger offspring compared to species with relatively low degrees of superfetation and matrotrophy (i.e. fewer simultaneous broods and lesser amounts of post-fertilization provisioning). Using different phylogenetic comparative methods and data on 44 species of viviparous fishes of the family Poeciliidae, we found a lack of association between offspring size and the combination of superfetation and matrotrophy. Therefore, the concurrent presence of superfetation and moderate or extensive matrotrophy has not facilitated the evolution of larger offspring. In fact, these traits have evolved differently. Superfetation and matrotrophy have accumulated gradual changes that largely can be explained by Brownian motion, whereas offspring size has evolved fluidly, experiencing changes that likely resulted from selective responses to the local conditions.

Species Selection Favors Dispersive Life Histories in Sea Slugs, but Higher Per-Offspring Investment Drives Shifts to Short-Lived Larvae.

For 40 years, paleontological studies of marine gastropods have suggested that species selection favors lineages with short-lived (lecithotrophic) larvae, which are less dispersive than long-lived (planktotrophic) larvae. Although lecithotrophs appeared to speciate more often and accumulate over time in some groups, lecithotrophy also increased extinction rates, and tests for state-dependent diversification were never performed. Molecular phylogenies of diverse groups instead suggested lecithotrophs accumulate without diversifying due to frequent, unidirectional character change. Although lecithotrophy has repeatedly originated in most phyla, no adult trait has been correlated with shifts in larval type. Thus, both the evolutionary origins of lecithotrophy and its consequences for patterns of species richness remain poorly understood. Here, we test hypothesized links between development mode and evolutionary rates using likelihood-based methods and a phylogeny of 202 species of gastropod molluscs in Sacoglossa, a clade of herbivorous sea slugs. Evolutionary quantitative genetics modeling and stochastic character mapping supported 27 origins of lecithotrophy. Tests for correlated evolution revealed lecithotrophy evolved more often in lineages investing in extra-embryonic yolk, the first adult trait associated with shifts in development mode across a group. However, contrary to predictions from paleontological studies, species selection actually favored planktotrophy; most extant lecithotrophs originated through recent character change, and did not subsequently diversify. Increased offspring provisioning in planktotrophs thus favored shifts to short-lived larvae, which led to short-lived lineages over macroevolutionary time scales. These findings challenge long-standing assumptions about the effects of alternative life histories in the sea. Species selection can explain the long-term persistence of planktotrophy, the ancestral state in most clades, despite frequent transitions to lecithotrophy.

Comparative life histories of fishes in the subgenus Limia (Pisces: Poeciliidae).

This study presents life-history descriptions for 12 species in the subgenus Limia, which are endemic to the Greater Antilles. All species in this study lack evidence of superfoetation, producing a single brood of offspring before developing subsequent broods. Interbrood intervals (number of days between parturition events) are also consistent with intervals of species that lack superfoetation. Maternal provisioning, characterized by matrotrophy index, is <1.0 for all species of Limia. This is consistent with species that provide little or no maternal provisioning to developing embryos after ovum fertilization (lecithotrophic). Four species exhibit potentially bi-modal size distributions of mature males. Work on other poeciliids suggests that such bimodal distributions can be caused by genetic polymorphisms in some species. Principle component analyses revealed an axis of interspecific variation in life histories that separated species with small size at maturity and the production of many, small offspring from those with large size at maturity and that produce few, large offspring. This pattern of life-history diversity occurs in many other groups of organisms.