Phylogenetic analyses of mode of larval development

Phylogenies based on morphological or molecular characters have been used to provide an evolutionary context for analysis of larval evolution. Studies of gastropods, bivalves, tunicates, sea stars, sea urchins, and polychaetes have revealed massive parallel evolution of similar larval forms. Some of these studies were designed to test, and have rejected, the species selection hypothesis for evolutionary trends in the frequency of derived larvae or life history traits. However, the lack of well supported models of larval character evolution leave some doubt about the quality of inferences of larval evolution from phylogenies of living taxa. Better models based on maximum likelihood methods and known prior probabilities of larval character state changes will improve our understanding of the history of larval evolution.     

It's about time: divergence, demography, and the evolution of developmental modes in marine invertebrates

Differences in larval developmental mode are predicted to affect ecological and evolutionary processes ranging from gene flow and population bottlenecks to rates of population recovery from anthropogenic disturbance and capacity for local adaptation. The most powerful tests of these predictions use comparisons among species to ask how phylogeographic patterns are correlated with the evolution and loss of prolonged planktonic larval development. An important and largely untested assumption of these studies is that interspecific differences in population genetic structure are mainly caused by differences in dispersal and gene flow (rather than by differences in divergence times among populations or changes in effective population sizes), and that species with similar patterns of spatial genetic variation have similar underlying temporal demographic histories. Teasing apart these temporal and spatial patterns is important for understanding the causes and consequences of evolutionary changes in larval developmental mode. New analytical methods that use the coalescent history of allelic diversity can reveal these temporal patterns, test the strength of traditional population-genetic explanations for variation in spatial structure based on differences in dispersal, and identify strongly supported alternative explanations for spatial structure based on demographic history rather than on gene flow alone. We briefly review some of these recent analytical developments, and show their potential for refining ideas about the correspondence between the evolution of larval developmental mode, population demographic history, and spatial genetic variation.     

The effect of developmental nutrition on life span and fecundity depends on the adult reproductive environment in Drosophila melanogaster

Both developmental nutrition and adult nutrition affect life‐history traits; however, little is known about whether the effect of developmental nutrition depends on the adult environment experienced. We used the fruit fly to determine whether life‐history traits, particularly life span and fecundity, are affected by developmental nutrition, and whether this depends on the extent to which the adult environment allows females to realize their full reproductive potential. We raised flies on three different developmental food levels containing increasing amounts of yeast and sugar: poor, control, and rich. We found that development on poor or rich larval food resulted in several life‐history phenotypes indicative of suboptimal conditions, including increased developmental time, and, for poor food, decreased adult weight. However, development on poor larval food actually increased adult virgin life span. In addition, we manipulated the reproductive potential of the adult environment by adding yeast or yeast and a male. This manipulation interacted with larval food to determine adult fecundity. Specifically, under two adult conditions, flies raised on poor larval food had higher reproduction at certain ages – when singly mated this occurred early in life and when continuously mated with yeast this occurred during midlife. We show that poor larval food is not necessarily detrimental to key adult life‐history traits, but does exert an adult environment‐dependent effect, especially by affecting virgin life span and altering adult patterns of reproductive investment. Our findings are relevant because (1) they may explain differences between published studies on nutritional effects on life‐history traits; (2) they indicate that optimal nutritional conditions are likely to be different for larvae and adults, potentially reflecting evolutionary history; and (3) they urge for the incorporation of developmental nutritional conditions into the central life‐history concept of resource acquisition and allocation.     

Genetic Variation and the Role of Insect Life History Traits in the Ability of Drosophila Larvae to Develop in the Presence of a Competing Filamentous Fungus

Competitive interactions between organisms from distantly related phylogenetical branches have been suggested as being one of the most pervasive forms of interspecific competition. However, so-called inter-kingdom competition has rarely been the focus of ecological and evolutionary studies. Thus, a relatively novel hypothesis has been proposed on the basis that saprophagous insects might intensively compete with filamentous fungi for ephemeral resources (e.g. decaying plant tissue). Consideration that life history traits (e.g. developmental time) are adaptive in determining developmental success in the presence of con- or hetero-specifics competitors implies that these traits have been progressively established by natural selection. Because a similar scenario may apply to antagonistic interactions between saprophagous insects and filamentous fungi, one can expect the existence of heritable variation in developmental success when insect larvae are forced to grow in the presence of noxious mould. Therefore, this study aimed at discovering whether a local population of Drosophila melanogaster indeed harbours genetic variation in developmental success in the presence of the mould Aspergillus niger. By using the isofemale line technique, single larvae forced to feed on fungal infected or uninfected substrate were analysed for variation in survival probability to the adult stage, developmental time and body size of emerged adults. I found genetic variation in survival probability in fungal infected substrates but not in uninfected larval food sources. Mean developmental time and body size varied significantly among isofemale lines in both types of larval environment. Survival was negatively correlated with developmental time on fungal infected substrate, but variation in developmental time on fungal-free substrates was not correlated with survival on fungal infected food patches. Within-trait correlation between fungal infected and uninfected substrates was surprisingly weak, and developmental time was not correlated with body size. The results of this study demonstrate (a) the existence of genetic variation for larval developmental success in the presence of A. niger in a Drosophila population, and (b) heritability of important insect life history traits differed as a function of the larval environment (fungal infected or uninfected feeding substrate). I discuss models that might explain heritability differences and the evolutionary consequences of these results.     

The active evolutionary lives of echinoderm larvae

Echinoderms represent a researchable subset of a dynamic larval evolutionary cosmos. Evolution of echinoderm larvae has taken place over widely varying time scales from the origins of larvae of living classes in the early Palaeozoic, approximately 500 million years ago, to recent, rapid and large-scale changes that have occurred within living genera within a span of less than a million years to a few million years. It is these recent evolutionary events that offer a window into processes of larval evolution operating at a micro-evolutionary level of evolution of discrete developmental mechanisms. We review the evolution of the diverse larval forms of living echinoderms to outline the origins of echinoderm larval forms, their diversity among living echinoderms, molecular clocks and rates of larval evolution, and finally current studies on the roles of developmental regulatory mechanisms in the rapid and radical evolutionary changes observed between closely related congeneric species.     

Functional design in the evolution of embryos and larvae

A function of development is to put the right kind of cells in the right place at the right time. Other functional analyses help define what is right. As examples, functional analyses offer explanations for the unicellular bottleneck in life histories that necessitates embryos, evolutionary divergences in embryonic cell cycles, conditions permissive of loss of larval structures and consequent change in embryonic development, and the decoupled development of larval bodies and juvenile rudiments. Functional analyses also reveal the specifications required of morphogenesis, hence defining developmental phenomena to be explained.     

Major muscle systems in the larval caenogastropod,Ilyanassa obsoleta,display different patterns of development

This study describes the anatomical and developmental aspects of muscular development from the early embryo to competent larval stage in the gastropod Ilyanassa obsoleta. Staining of F‐actin revealed differential spatial and temporal patterns of several muscles. In particular, two major muscles, the larval retractor and pedal retractor muscles originate independently and display distinct developmental patterns similar to observations in other gastropod species. Additionally, together with the larval retractor muscle, the accessory larval muscle developed in the embryo at the trochophore stage. Therefore, both these muscles develop prior to ontogenetic torsion. The pedal retractor muscle marked the most abundant growth in the mid veliger stage. Also during the middle stage, the metapodial retractor muscle and opercular retractor muscle grew concurrently with development of the foot. We show evidence that juvenile muscles, such as the buccal mass muscle and siphon muscle develop initially during the late veliger stage. Collectively, these findings substantiate that larval myogenesis involves a complex sequence of events that appear evolutionary conserved within the gastropods, and set the stage for future studies using this model species to address issues concerning the evolution and eventual fates of larval musculature in molluscs. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Models of metamorphic timing: an experimental evaluation with the pond-dwelling salamander Hemidactylium scutatum (Caudata: Plethodontidae)

Amphibian larvae vary tremendously in size at metamorphosis and length of larval period. We raised pond-dwelling four-toed salamander (Hemidactylium scutatum) larvae to test two models that predict a larva’s age and size at metamorphosis. The Wilbur-Collins model proposes that the developmental rate of a larva responds to changes in growth rate in an adaptive manner throughout the larval period, and that metamorphosis can be initiated after a minimum size has been reached. The Leips-Travis or fixed-rate model states that developmental rate is set early in the larval period, perhaps by early growth rate or food availability and their positive correlation with developmental rate, and that changes in growth rate during the larval period affect size at metamorphosis, but have no effect on the age of an individual at metamorphosis. A modified version of the Wilbur-Collins model suggests that a larva’s developmental rate becomes fixed about two-thirds of the way through the larval period, with changes in growth rate after that point only affecting size at metamorphosis. Larvae were raised on eight different feeding regimes which created two constant and six variable growth histories. Growth history did significantly affect size at metamorphosis. However, an a posteriori statistical test revealed a group of seven and an overlapping group of six treatments with indistinguishable lengths of larval period, indicating a general picture of a fixed developmental rate regardless of growth history. This result is unique among similar studies on invertebrates, fish, and frogs. There was no association between early growth or food level and development rates. Neither the Wilbur-Collins nor the Leips-Travis fixed-rate models were supported. The invariable developmental rate of Hemidactylium and recent osteological evidence from the literature suggest that larvae begin the process of metamorphosis as soon as they hatch, probably a trait selected for by strong predation pressure in the aquatic environment. A variety of different approaches (ecological, developmental, phylogenetic) are necessary to fully evaluate the adaptive nature of the timing of transitions between life cycle stages. Received: 3 June 1999 / Accepted: 18 March 2000     

Evolution of complex life cycles of amphibians: bridging the gap between metapopulation dynamics and life history evolution

Current evolutionary models for amphibian life cycles reflect tradeoffs in size-specific growth and mortality rates between the aquatic and terrestrial stages. A limitation of these models is that they do not incorporate evolutionary phenomena that are associated with metapopulation structure. In this work I address components of the evolution of complex life cycles (CLCs) that are tied to the metapopulation dynamics of amphibians that use seasonal wetlands that vary in hydroperiod. In particular, I describe how selection for the minimum length of the larval period affects metapopulation viability and the selection/migration equilibrium. Selection to increase the minimum length of the larval period functionally reduces the number of viable breeding sites on the landscape, increases the average distance between neighboring sites, and increases the risk of metapopulation extinction. Within a metapopulation, asymmetric gene flow between populations that are adapted to different hydroperiods tends to swamp local selection for long larval periods at sites with long hydroperiods. The evolutionary stability of CLCs of many species with metapopulation structure may reflect the fact that extremely small metamorphs cannot survive on land, while lineages with long larval periods incur a high risk of metapopulation extinction. I encourage theorists to more carefully consider how life history traits and metapopulation viability are related for these and other taxa.     

Development and evolution of adult feeding structures in Caenogastropods: overcoming larval functional constraints

SUMMARY Comparative study of the developing foregut in three species of caenogastropods, including an herbivorous grazer ( Lacuna vincta ) and two carnivores ( Euspira [ Polinices ] lewisii and Nassarius mendicus ), suggests how the specialized adult foregut of a carnivorous neogastropod evolved within a life cycle having a planktotrophic larva. Postmetamorphic feeding structures (buccal cavity and radular sac) in all three species achieve advanced differentiation in the larval stage, permitting juvenile feeding at 3 days postmetamorphosis. Recent phylogenetic hypotheses for the Gastropoda predict that foregut developmental patterns in E. lewisii and N. mendicus are derived, relative to that of L. vincta. In hatching larvae of these three, the anlage of postmetamorphic feeding structures is a small patch of nonciliated cells embedded in the ventral wall of the larval foregut and the patch soon forms an outpocketing. During subsequent morphogenesis, Euspira lewisii and N. mendicus share a developmental novelty that involves semi-isolation of the developing, postmetamorphic buccal cavity and radular sac from the larval foregut and formation of a new, definitive mouth at metamorphosis. Nassarius mendicus , a neogastropod, embellishes this novelty by adding the entire anterior esophagus and valve of Leiblein ( de novo structures) to the semi-isolated buccal cavity. Therefore, a valve and long stretch of muscular anterior esophagus, which are necessary for feeding with a pleurembolic proboscis, are preformed in the larval stage of this neogastropod without interfering with larval feeding. The inferred evolutionary events leading to postmetamorphic feeding specialization in N. mendicus are invisible in adults; they require reconstruction from comparative developmental analysis.