Showing papers in "Integrative and Comparative Biology in 2012"

Reproductive output and duration of the pelagic larval stage determine seascape-wide connectivity of marine populations.

Abstract: Connectivity among marine populations is critical for persistence of metapopulations, coping with climate change, and determining the geographic distribution of species. The influence of pelagic larval duration (PLD) on connectivity has been studied extensively, but relatively little is known about the influence of other biological parameters, such as the survival and behavior of larvae, and the fecundity of adults, on population connectivity. Furthermore, the interaction between the seascape (habitat structure and currents) and these biological parameters is unclear. We explore these interactions using a biophysical model of larval dispersal across the Indo-Pacific. We describe an approach that quantifies geographic patterns of connectivity from demographically relevant to evolutionarily significant levels across a range of species. We predict that at least 95% of larval settlement occurs within 155 km of the source population and within 13 days irrespective of the species' life history, yet long-distant connections remain likely. Self-recruitment is primarily driven by the local oceanography, larval mortality, and the larval precompetency period, whereas broad-scale connectivity is strongly influenced by reproductive output (abundance and fecundity of adults) and the length of PLD. The networks we have created are geographically explicit models of marine connectivity that define dispersal corridors, barriers, and the emergent structure of marine populations. These models provide hypotheses for empirical testing.

Assessing the Impacts of Phenotypic Plasticity on Evolution

Abstract: In the past decade, there has been a resurgent interest in whether and how phenotypic plasticity might impact evolutionary processes. Of fundamental importance is how the environment influences individual phenotypic development while simultaneously selecting among phenotypic variants in a population. Conceptual and theoretical treatments of the evolutionary implications of plasticity are numerous, as are criticisms of the conclusions. As such, the time is ripe for empirical evidence to catch up with theoretical predictions. To this end, I provide a summary of eight hypotheses at the core of this issue, highlighting various approaches by which they can be tested. My goal is to provide practical guidance to those seeking to understand the complex ways by which phenotypic plasticity can influence evolutionary innovation and diversification.

Adaptive transgenerational plasticity in an annual plant: grandparental and parental drought stress enhance performance of seedlings in dry soil.

Abstract: Stressful parental (usually maternal) environments can dramatically influence expression of traits in offspring, in some cases resulting in phenotypes that are adaptive to the inducing stress. The ecological and evolutionary impact of such transgenerational plasticity depends on both its persistence across generations and its adaptive value. Few studies have examined both aspects of transgenerational plasticity within a given system. Here we report the results of a growth-chamber study of adaptive transgenerational plasticity across two generations, using the widespread annual plant Polygonum persicaria as a naturally evolved model system. We grew five inbred Polygonum genetic lines in controlled dry vs. moist soil environments for two generations in a fully factorial design, producing replicate individuals of each genetic line with all permutations of grandparental and parental environment. We then measured the effects of these two-generational stress histories on traits critical for functioning in dry soil, in a third (grandchild) generation of seedling offspring raised in the dry treatment. Both grandparental and parental moisture environment significantly influenced seedling development: seedlings of drought-stressed grandparents or parents produced longer root systems that extended deeper and faster into dry soil compared with seedlings of the same genetic lines whose grandparents and/or parents had been amply watered. Offspring of stressed individuals also grew to a greater biomass than offspring of nonstressed parents and grandparents. Importantly, the effects of drought were cumulative over the course of two generations: when both grandparents and parents were drought-stressed, offspring had the greatest provisioning, germinated earliest, and developed into the largest seedlings with the most extensive root systems. Along with these functionally appropriate developmental effects, seedlings produced after two previous drought-stressed generations had significantly greater survivorship in very dry soil than did seedlings with no history of drought. These findings show that plastic responses to naturalistic resource stresses experienced by grandparents and parents can "preadapt" offspring for functioning under the same stresses in ways that measurably influence realized fitness. Possible implications of these environmentally-induced, inherited adaptations are discussed with respect to ecological distribution, persistence under novel stresses, and evolution in natural populations.

The Integrated Phenotype

Abstract: Proper functioning of complex phenotypes requires that multiple traits work together. Examination of relationships among traits within and between complex characters and how they interact to function as a whole organism is critical to advancing our understanding of evolutionary developmental plasticity. Phenotypic integration refers to the relationships among multiple characters of a complex phenotype, and their relationships with other functional units (modules) in an organism. In this review, I summarize a brief history of the concept of phenotypic integration in plant and animal biology. Following an introduction of concepts, including modularity, I use an empirical case-study approach to highlight recent advance in clarifying the developmental and genomic basis of integration. I end by highlighting some novel approaches to genomic and epigenetic perturbations that offer promise in further addressing the role of phenotypic integration in evolutionary diversification. In the age of the phenotype, studies that examine the genomic and developmental changes in relationships of traits across environments will shape the next chapter in our quest for understanding the evolution of complex characters.

Twenty-Four Years in the Mud: What Have We Learned About the Natural History and Ecology of the Mangrove Rivulus, Kryptolebias marmoratus?

Abstract: Although first described in 1880, Kryptolebias marmoratus avoided scientific scrutiny until 1961, when it was identified as the only known selfing hermaphroditic vertebrate. The subsequent intense interest in this fish as a laboratory animal, continuing to this day, might explain the paucity of wild collections, but our collective knowledge now suggests that the inherent difficulty of wild collection is more a matter of "looking in all the wrong places." Long thought to be rare in the mangroves, and it is rare in certain human-impacted habitats, K. marmoratus can be quite abundant, but in microhabitats not typically targeted by ichthyologists: ephemeral pools at higher elevations in the swamp, crab burrows, and other fossorial or even terrestrial haunts. Field studies of this enigmatic fish have revealed almost amphibious behaviors. During emersion these fish tolerate extended dry periods. In water, they are exposed to temperature extremes, high levels of hydrogen sulfide, and depleted dissolved oxygen. Finally, their catholic diet and a geographically variable sex life completes a portrait of an unusual animal. A clearer picture is emerging of adult life, with initial population density estimates now known and some indication of high population turnover in burrows, but juvenile habitat and adult oviposition sites remain unknown.

Dispersal of Deep-Sea Larvae from the Intra-American Seas: Simulations of Trajectories using Ocean Models

Abstract: Using data on ocean circulation with a Lagrangian larval transport model, we modeled the potential dispersal distances for seven species of bathyal invertebrates whose durations of larval life have been estimated from laboratory rearing, MOCNESS plankton sampling, spawning times, and recruitment. Species associated with methane seeps in the Gulf of Mexico and/or Barbados included the bivalve "Bathymodiolus" childressi, the gastropod Bathynerita naticoidea, the siboglinid polychaete tube worm Lamellibrachia luymesi, and the asteroid Sclerasterias tanneri. Non-seep species included the echinoids Cidaris blakei and Stylocidaris lineata from sedimented slopes in the Bahamas and the wood-dwelling sipunculan Phascolosoma turnerae, found in Barbados, the Bahamas, and the Gulf of Mexico. Durations of the planktonic larval stages ranged from 3 weeks in lecithotrophic tubeworms to more than 2 years in planktotrophic starfish. Planktotrophic sipunculan larvae from the northern Gulf of Mexico were capable of reaching the mid-Atlantic off Newfoundland, a distance of more than 3000 km, during a 7- to 14-month drifting period, but the proportion retained in the Gulf of Mexico varied significantly among years. Larvae drifting in the upper water column often had longer median dispersal distances than larvae drifting for the same amount of time below the permanent thermocline, although the shapes of the distance-frequency curves varied with depth only in the species with the longest larval trajectories. Even species drifting for >2 years did not cross the ocean in the North Atlantic Drift.

Barnacles and Biofouling

Abstract: Biofouling, the attachment and growth of organisms on submerged, man-made surfaces, has plagued ship operators for at least 2500 years. Accumulation of biofouling, including barnacles and other sessile marine invertebrates, increases the frictional resistance of ships' hulls, resulting in an increase in power and in fuel consumption required to make speed. Scientists and engineers recognized over 100 years ago that in order to solve the biofouling problem, a deeper understanding of the biology of the organisms involved, particularly with regard to larval settlement and metamorphosis and adhesives and adhesion, would be required. Barnacles have served as an important tool in pursuing this research. Over the past 20 years, the pace of these studies has accelerated, likely driven by the introduction of environmental regulations banning the most effective biofouling control products from the market. Research has largely focused on larval settlement and metamorphosis, the development of new biocides, and materials/surface science. Increased research has so far, however, failed to result in commercial applications. Two recent successes (medetomidine/Selektope(®), surface-bound noradrenaline) build on our improving understanding of the role of the larval nervous system in mediating settlement and metamorphosis. New findings with regard to the curing of barnacle adhesives may pave the way to additional successes. Although the development of most current biofouling control technologies remains largely uninfluenced by basic research on, for example, the ability of settling larvae to perceive surface cues, or the nature of the interaction between organismal adhesives and the substrate, newly-developed materials can serve as useful probes to further our understanding of these processes.

Passive robotic models of propulsion by the bodies and caudal fins of fish.

Abstract: Considerable progress in understanding the dynamics of fish locomotion has been made through studies of live fishes and by analyzing locomotor kinematics, muscle activity, and fluid dynamics. Studies of live fishes are limited, however, in their ability to control for parameters such as length, flexural stiffness, and kinematics. Keeping one of these factors constant while altering others in a repeatable manner is typically not possible, and it is difficult to make critical measurements such as locomotor forces and torques on live, freely-swimming fishes. In this article, we discuss the use of simple robotic models of flexing fish bodies during self-propulsion. Flexible plastic foils were actuated at the leading edge in a heave and/or pitch motion using a robotic flapping controller that allowed moving foils to swim at their self-propelled speed. We report unexpected non-linear effects of changing the length and stiffness of the foil, and analyze the effect of changing the shape of the trailing edge on self-propelled swimming speed and kinematics. We also quantify the structure of the wake behind swimming foils with volumetric particle image velocimetry, and describe the effect of flexible heterocercal and homocercal tail shapes on flow patterns in the wake. One key advantage of the considerable degree of control afforded by robotic devices and the use of simplified geometries is the facilitation of mathematical analyses and computational models, as illustrated by the application of an inviscid computational model to propulsion by a flapping foil. This model, coupled with experimental data, demonstrates an interesting resonance phenomenon in which swimming speed varies with foil length in an oscillatory manner. Small changes in length can have dramatic effects on swimming speed, and this relationship changes with flexural stiffness of the swimming foil.

Selective processes in development: implications for the costs and benefits of phenotypic plasticity.

Abstract: Adaptive phenotypic plasticity, the ability of a genotype to develop a phenotype appropriate to the local environment, allows organisms to cope with environmental variation and has implications for predicting how organisms will respond to rapid, human-induced environmental change. This review focuses on the importance of developmental selection, broadly defined as a developmental process that involves the sampling of a range of phenotypes and feedback from the environment reinforcing high-performing phenotypes. I hypothesize that understanding the degree to which developmental selection underlies plasticity is key to predicting the costs, benefits, and consequences of plasticity. First, I review examples that illustrate that elements of developmental selection are common across the development of many different traits, from physiology and immunity to circulation and behavior. Second, I argue that developmental selection, relative to a fixed strategy or determinate (switch) mechanisms of plasticity, increases the probability that an individual will develop a phenotype best matched to the local environment. However, the exploration and environmental feedback associated with developmental selection is costly in terms of time, energy, and predation risk, resulting in major changes in life history such as increased duration of development and greater investment in individual offspring. Third, I discuss implications of developmental selection as a mechanism of plasticity, from predicting adaptive responses to novel environments to understanding conditions under which genetic assimilation may fuel diversification. Finally, I outline exciting areas of future research, in particular exploring costs of selective processes in the development of traits outside of behavior and modeling developmental selection and evolution in novel environments.

Dispersal in Marine Organisms without a Pelagic Larval Phase

Abstract: Synopsis In contrast to marine organisms whose offspring go through an extended planktonic stage, the young of others develop directly into benthic juveniles or into yolky nonfeeding larvae that spend only a few hours in the plankton before settling. Yet, paradoxically, many such species have geographic distributions that are comparable to those with a pelagic dispersal stage. This article reviews some of the ways in which these organisms can expand their distributions: drifting, rafting, hitchhiking, creeping, and hopping. Drifting applies to species in which larvae may be short-lived, but adults can detach or be detached from their benthic substratum and be passively carried to new areas, floating at the water’s surface or below it. Many encrusting species and mobile species can spread by rafting, settling on natural or artificial floating substrata which are propelled by wind and currents to new regions. Hitchhiking applies to those attaching to vessels or being carried in ballast water of ships to a distant region in which their offspring can survive. Other marine species extend their distributions by hopping from one island of hard substratum or favorable sedimentary microhabitat to another, while creeping species extend their distributions along shores or shelves where habitats remain similar for long distances.

What controls connectivity? An empirical, multi-species approach.

Abstract: Synopsis The exchange of individuals among habitat patches (connectivity) has broad relevance for the conservation and management of marine metapopulations. Elemental fingerprinting-based research conducted over the past 12 years along the open coastline and bays of San Diego County in southern California evaluated connectivity patterns for seven species: one native and two invasive mussels, an oyster, a brachyuran crab, and two fishes. The studies spanned different years and seasons but overlapped considerably in space, allowing comparisons of dispersal patterns across species, and assessment of the relative importance of location, circulation, and intra-annual and inter-annual variability. We asked whether the species exhibited commonalities in directional transport, transport distances, sources and sinks, self-recruitment, and bay-ocean exchange. Linked connectivity-demographic analyses conducted for two species of mytilid mussels and two fishes allowed evaluation of the contributions of realized connectivity to metapopulation dynamics relative to other life-history attributes. Common trends across species include average along-shore dispersal distances of 15–35 km and seasonal changes in direction of dispersal that mirrored patterns of along-shore circulation. We observed greater isolation of back-bay populations, significant exchange from front bay to ocean, and high self-recruitment in locations on the northern, open coast, and in the southern bays. Connectivity was rarely the most influential driver of growth and persistence of metapopulations, but influenced the importance of other vital rates. Several locations served consistently as sources of larvae or as nurseries for multiple species, but there were few sites in common that were sinks. For the mussels, reproductive timing guided directional transport. These results imply that local management (e.g., habitat protection, opening of the mouths of lagoons, location of aquaculture farms) may be effective along this coastline. Regional, multi-species assessments of exchange of larvae should move us closer to ecosystem-based management.

Environmental Proteomics of the Mussel Mytilus: Implications for Tolerance to Stress and Change in Limits of Biogeographic Ranges in Response to Climate Change

Abstract: Climate change will affect temperature extremes and averages, and hyposaline conditions in coastal areas due to extreme precipitation events and oceanic pH. How climate change will push species close to, or beyond, their physiological tolerance limits as well as change the limits of their biogeographic ranges can probably be investigated best in species that have already responded to climate change and whose distribution ranges are currently in flux. Blue mussels provide such a study system, with the invading warm-adapted Mediterranean Mytilus galloprovincialis having replaced the native more cold-adapted Mytilus trossulus from the southern part of its range in southern California over the past century, possibly due to climate change. However, freshwater input may prevent the latter species from expanding further north. We used a proteomics approach to characterize the responses of the two congeners to acute heat stress, chronic thermal acclimation, and hyposaline stress. In addition, we investigated the proteomic changes in response to decreasing seawater pH in another bivalve, the eastern oyster Crassostrea virginica. The results suggest that reactive oxygen species (ROS) are a common costressor during environmental stress, including oceanic acidification, and possibly cause modifications of cytoskeletal elements. All stressors disrupted protein homeostasis, indicated by the induction of molecular chaperones and, in the case of acute heat stress, proteasome isoforms, possibly due both to protein denaturation directly by the stressor and to the production of ROS. Acute stress by heat and hyposalinity changed several small G-proteins implicated in cytoskeletal modifications and vesicular transport, respectively. Changes in abundance of proteins involved in energy metabolism and ROS scavenging further suggest a possible trade-off during acute and chronic stress from heat and cold between ROS-generating NADH-producing pathways and ROS-scavenging NADPH-producing pathways, especially through the reaction of NADPH-dependent isocitrate dehydrogenase and the pentose-phosphate pathway. Some of the proteomic changes may not constitute de novo protein synthesis but rather shifts in abundance of isoforms differing in posttranslational modifications, specifically acetylation by a NAD-dependent deacetylase (sirtuin). Interspecific differences suggest that these processes set physiological tolerance limits and thereby contribute to recent biogeographic shifts in range, possibly caused by climate change.

Effects of Capability for Dispersal on the Evolution of Diversity in Antarctic Benthos

Abstract: The likelihood of marine invertebrates to maintain large geographic ranges is widely dependent on the ability of their early ontogenetic stages to disperse over long distances. Marine benthic invertebrates inhabiting the cold-stenothermal environment of the Southern Ocean are known for their overall reduced number of pelagic larvae, or drifting stages of any kind, when compared with organisms elsewhere in the sea. The diversity of organisms thriving in Antarctic waters is the result of evolution in situ and of the intrusion of species from surrounding seas. The reasons for a high level of endemism and a stunning diversity of benthic invertebrates found today are frequently discussed in the literature, but the mechanisms whereby diversity has been controlled over time remain largely theoretical. Here, I suggest that, indeed, early life-history patterns play a key role in defining the radiation and the speciation potential of Antarctic benthic invertebrates. In arguing this case, I synthesize the growing body of molecular studies on population connectivity in Antarctic benthic invertebrates, and compare this information with knowledge of their life histories and biogeography. I conclude that differences in early life-history patterns are key to the resilience potential of species in response to late Cenozoic glacial periods and propose that there is a direct relationship between rate of speciation and the ability of taxa to disperse.

Aggression and related behavioral traits: the impact of winning and losing and the role of hormones.

Abstract: Synopsis A suite of correlated behaviors reflecting between-individual consistency in behavior across multiple situations is termed a ‘‘behavioral syndrome.’’ Researchers have suggested that a cause for the correlation between different behaviors might lie in the neuroendocrine system. In this study, we examined the relationships between aggressiveness (a fish’s readiness to perform gill display to its mirror image) and each of boldness (the readiness to emerge from a shelter), exploratory tendency (the readiness to approach a novel shelter), and learning performance (the probability of entering the correct reservoir in a T-maze test) in a mangrove rivulus, Kryptolebias marmoratus. We explored the possibility that the relationships between them arise because these behaviors are all modulated by cortisol and testosterone. We also tested the stability of the relationships between these behaviors shortly after using a winning or losing experience to alter individuals’ aggressiveness. The results were that aggressiveness correlated positively with boldness and the tendency to explore, and that these three behavioral traits were all positively correlated with pre-experience testosterone levels. Aggressiveness and boldness also positively correlated with pre-experience cortisol levels; exploratory tendency did not. The relationship between aggressiveness and boldness appeared to be stronger than that between either of them and exploratory tendency. These results suggest that testosterone and cortisol play important roles in mediating the correlations between these behavioral traits. Learning performance was not significantly correlated with the other behavioral traits or with levels of testosterone or cortisol. Recent experience in contests influenced individuals’ aggressiveness, tendency to explore, and learning performance but not their boldness; individuals that received a winning experience were quicker to display to their mirror image and performed better in the learning task but were slower to approach a novel object than were individuals that lost. Contest experience did not, however, significantly influence the relationships between aggressiveness and any of boldness, exploratory tendency, or learning performance. The results show that the individual components of a suite of correlated behaviors can preserve a flexibility to respond differently to environmental stimuli.

Exploring Androgen-Regulated Pathways in Teleost Fish Using Transcriptomics and Proteomics

Abstract: In the environment, there are aquatic pollutants that disrupt androgen signaling in fish. Laboratory and field-based experiments have utilized omics technologies to characterize the molecular mechanisms underlying androgen-receptor agonism/antagonism. Transcriptomics and proteomics studies with 17β-trenbolone, a growth-promoting pharmaceutical found in water systems surrounding cattle feed lots, and androgens such as 17α-methyltestosterone and 17α-methyldihydrotestosterone, have been conducted in ovary and liver of fish that include the fathead minnow (FHM) (Pimephales promelas), common carp (Cyprinus carpio), Qurt medaka (Oryzias latipes), and zebrafish (Danio rerio). In this mini-review, we survey recent omics studies in fish and reveal that, despite the diversity of species and tissues examined, there are common cellular responses that are observed with waterborne androgenic treatments. Recurring themes in gene ontology include apoptosis, transport and oxidation of lipids, synthesis and transport of hormones, immune response, protein metabolism, and cell proliferation. However, we also discuss other mechanisms other than androgen receptor (AR) activation, such as responses to toxicant stress, estrogen receptor agonism, aromatization of androgens into estrogens, and inhibitory feedback mechanisms by high levels of androgens that may also explain molecular responses in fish. To further explore androgen-responsive protein networks, a sub-network enrichment analysis was performed on protein data collected from the livers of female FHMs exposed to 17β-trenbolone. We construct a putative AR-regulated protein/cell process network in the liver that includes B-lymphocyte differentiation, xenobiotic clearance, low-density lipoprotein oxidation, proliferation of smooth muscle cells, and permeability of blood vessels. We demonstrate that construction of protein networks can offer insight into cell processes that are potentially regulated by androgens.

Relaxed Genetic Constraint is Ancestral to the Evolution of Phenotypic Plasticity

Abstract: Phenotypic plasticity––the capacity of a single genotype to produce different phenotypes in response to varying environmental conditions––is widespread. Yet, whether, and how, plasticity impacts evolutionary diversification is unclear. According to a widely discussed hypothesis, plasticity promotes rapid evolution because genes expressed differentially across different environments (i.e., genes with “biased” expression) experience relaxed genetic constraint and thereby accumulate variation faster than do genes with unbiased expression. Indeed, empirical studies confirm that biased genes evolve faster than unbiased genes in the same genome. An alternative hypothesis holds, however, that the relaxed constraint and faster evolutionary rates of biased genes may be a precondition for, rather than a consequence of, plasticity’s evolution. Here, we evaluated these alternative hypotheses by characterizing evolutionary rates of biased and unbiased genes in two species of frogs that exhibit a striking form of phenotypic plasticity. We also characterized orthologs of these genes in four species of frogs that had diverged from the two plastic species before the plasticity evolved. We found that the faster evolutionary rates of biased genes predated the evolution of the plasticity. Furthermore, biased genes showed greater expression variance than did unbiased genes, suggesting that they may be more dispensable. Phenotypic plasticity may therefore evolve when dispensable genes are co-opted for novel function in environmentally induced phenotypes. Thus, relaxed genetic constraint may be a cause––not a consequence––of the evolution of phenotypic plasticity, and thereby contribute to the evolution of novel traits.

Using computational and mechanical models to study animal locomotion.

Abstract: Recent advances in computational methods have made realistic large-scale simulations of animal locomotion possible. This has resulted in numerous mathematical and computational studies of animal movement through fluids and over substrates with the purpose of better understanding organisms’ performance and improving the design of vehicles moving through air and water and on land. This work has also motivated the development of improved numerical methods and modeling techniques for animal locomotion that is characterized by the interactions of fluids, substrates, and structures. Despite the large body of recent work in this area, the application of mathematical and numerical methods to improve our understanding of organisms in the context of their environment and physiology has remained relatively unexplored. Nature has evolved a wide variety of fascinating mechanisms of locomotion that exploit the properties of complex materials and fluids, but only recently are the mathematical, computational, and robotic tools available to rigorously compare the relative advantages and disadvantages of different methods of locomotion in variable environments. Similarly, advances in computational physiology have only recently allowed investigators to explore how changes at the molecular, cellular, and tissue levels might lead to changes in performance at the organismal level. In this article, we highlight recent examples of how computational, mathematical, and experimental tools can be combined to ultimately answer the questions posed in one of the grand challenges in organismal biology: “Integrating living and physical systems.”

Proteomics to Assess the Role of Phenotypic Plasticity in Aquatic Organisms Exposed to Pollution and Global Warming

Abstract: Nowadays, the unprecedented rates of anthropogenic changes in ecosystems suggest that organisms have to migrate to new distributional ranges or to adapt commensurately quickly to new conditions to avoid becoming extinct. Pollution and global warming are two of the most important threats aquatic organisms will have to face in the near future. If genetic changes in a population in response to natural selection are extensively studied, the role of acclimation through phenotypic plasticity (the property of a given genotype to produce different phenotypes in response to particular environmental conditions) in a species to deal with new environmental conditions remains largely unknown. Proteomics is the extensive study of the protein complement of a genome. It is dynamic and depends on the specific tissue, developmental stage, and environmental conditions. As the final product of gene expression, it is subjected to several regulatory steps from gene transcription to the functional protein. Consequently, there is a discrepancy between the abundance of mRNA and the abundance of the corresponding protein. Moreover, proteomics is closer to physiology and gives a more functional knowledge of the regulation of gene expression than does transcriptomics. The study of protein-expression profiles, however, gives a better portrayal of the cellular phenotype and is considered as a key link between the genotype and the organismal phenotype. Under new environmental conditions, we can observe a shift of the protein-expression pattern defining a new cellular phenotype that can possibly improve the fitness of the organism. It is now necessary to define a proteomic norm of reaction for organisms acclimating to environmental stressors. Its link to fitness will give new insights into how organisms can evolve in a changing environment. The proteomic literature bearing on chronic exposure to pollutants and on acclimation to heat stress in aquatic organisms, as well as potential application of proteomics in evolutionary issues, are outlined. While the transcriptome responses are commonly investigated, proteomics approaches now need to be intensified, with the new perspective of integrating the cellular phenotype with the organismal phenotype and with the mechanisms of the regulation of gene expression, such as epigenetics.

The Nature of Nurture and the Future of Evodevo: Toward a Theory of Developmental Evolution

Abstract: This essay has three parts. First, I posit that much research in contemporary evodevo remains steeped in a traditional framework that views traits and trait differences as being caused by genes and genetic variation, and the environment as providing an external context in which development and evolution unfold. Second, I discuss three attributes of organismal development and evolution, broadly applicable to all organisms and traits that call into question the usefulness of gene- and genome-centric views of development and evolution. I then focus on the third and main aim of this essay and ask: what conceptual and empirical opportunities exist that would permit evodevo research to transcend the traditional boundaries inherited from its parent disciplines and to move toward the development of a more comprehensive and realistic theory of developmental evolution? Here, I focus on three conceptual frameworks, the theory of facilitated variation, the theory of evolution by genetic accommodation, and the theory of niche construction. I conclude that combined they provide a rich, interlocking framework within which to revise existing and develop novel empirical approaches toward a better understanding of the nature of developmental evolution. Examples of such approaches are highlighted, and the consequences of expanding existing frameworks are discussed.

Phenotypic Plasticity and Integration in the Mangrove Rivulus (Kryptolebias marmoratus): A Prospectus

Abstract: The mangrove rivulus (Kryptolebias marmoratus) is a small fish native to mangrove ecosystems in Florida, the Caribbean, Central America, and South America. This species is one of only two self-fertilizing, hermaphroditic vertebrates capable of producing offspring that are genetically identical to both the parent and all siblings. Long bouts of selfing result in individuals with completely homozygous genotypes, effectively allowing for the production of “clones.” Rivulus is also extremely sensitive to environmental change, both during development and adulthood. Life-history traits, behavior, physiology, morphology, and even sexual phenotype are shaped to a large extent by the interaction of genes with the environment, and many of these traits appear to co-vary. True reaction norms can be generated for this species in much the same way as has been done for clonally reproducing invertebrates and plants that have contributed immensely to our understanding of the evolution of phenotypic plasticity. That is, rivulus provides the opportunity to place individuals with identical genotypes in many different environments at any point during ontogeny or adulthood. In addition, rivulus populations are characterized by high genotypic diversity, a luxury not afforded by many clonal vertebrates, which allows us to evaluate variation among genotypes in the shape of reaction norms and in patterns of covariance among traits. We provide background information on phenotypic plasticity and phenotypic integration, coupled with a description of characteristics that we feel qualify rivulus as a potentially powerful model in which to study the evolution of reaction norms and covariance among traits.

Paratransgenesis: An approach to improve colony health and molecular insight in honey bees (Apis mellifera)?

Abstract: The honey bee (Apis mellifera) is highly valued as a commercial crop pollinator and a model animal in research. Over the past several years, governments, beekeepers, and the general public in the United States and Europe have become concerned by increased losses of honey bee colonies, calling for more research on how to keep colonies healthy while still employing them extensively in agriculture. The honey bee, like virtually all multicellular organisms, has a mutually beneficial relationship with specific microbes. The microbiota of the gut can contribute essential nutrients and vitamins and prevent colonization by non-indigenous and potentially harmful species. The gut microbiota is also of interest as a resource for paratransgenesis; a Trojan horse strategy based on genetically modified symbiotic microbes that express effector molecules antagonizing development or transmission of pathogens. Paratransgenesis was originally engineered to combat human diseases and agricultural pests that are vectored by insects. We suggest an alternative use, as a method to promote health of honey bees and to expand the molecular toolbox for research on this beneficial social insect. The honey bees' gut microbiota contains lactic acid bacteria including the genus Lactobacillus that has paratransgenic potential. We present a strategy for transforming one Lactobacillus species, L. kunkeei, for use as a vector to promote health of honey bees and functional genetic research.

Microevolutionary Distribution of Isogenicity in a Self-fertilizing Fish (Kryptolebias marmoratus) in the Florida Keys

Abstract: The mangrove rivulus Kryptolebias marmoratus and a closely related species are the world's only vertebrates that routinely self-fertilize. Such uniqueness presents a model for understanding why this reproductive mode, common in plants and invertebrates, is so rare in vertebrates. A survey of 32 highly polymorphic loci in >200 specimens of mangrove rivulus from multiple locales in the Florida Keys, USA, revealed extensive population-genetic structure on microspatial and micro-temporal scales. Observed heterozygosities were severely constrained, as expected for a hermaphroditic species with a mixed-mating system and low rates of outcrossing. Despite the pronounced population structure and the implied restrictions on effective gene flow, isogenicity (genetic identity across individuals) within and among local inbred populations was surprisingly low even after factoring out probable de novo mutations. Results indicate that neither frequent bottlenecks nor directional genetic adaptation to local environmental conditions were the primary driving forces impacting multilocus population-genetic architecture in this self-fertilizing vertebrate species. On the other hand, a high diversity of isogenic lineages within relatively small and isolated local populations is consistent with the action of diversifying selection driven by the extreme spatio-temporal environmental variability that is characteristic of mangrove habitats.

Biomechanics of larval morphology affect swimming: insights from the sand dollars Dendraster excentricus.

Abstract: Synopsis Most planktonic larvae of marine invertebrates are denser than sea water, and rely on swimming to locate food, navigate advective currents, and avoid predators. Therefore, swimming behaviors play important roles in larval survival and dispersal. Larval bodies are often complex and highly variable across developmental stages and environmental conditions. These complex morphologies reflect compromises among multiple evolutionary pressures, including maintaining the ability to swim. Here, I highlight metrics of swimming performance, their relationships with morphology, and the roles of behavior in modulating larval swimming within biomechanical limits. Sand dollars have a representative larval morphology using long ciliated projections for swimming and feeding. Observed larval sand dollars fell within a narrow range of key morphological parameters that maximized their abilities to maintain directed upward movement over the most diverse flow fields, outperforming hypothetical alternatives in a numerical model. Ontogenetic changes in larval morphology also led to different vertical movements in simulated flow fields, implying stage-dependent vertical distributions and lateral transport. These model outcomes suggest a tight coupling between larval morphology and swimming. Environmental stressors, such as changes in temperature and pH, can therefore affect larval swimming through short-term behavioral adjustments and long-term changes in morphology. Larval sand dollars reared under elevated pCO2 conditions had significantly different morphology, but not swimming speeds or trajectories. Geometric morphometric analysis showed a pH-dependent, size-mediated change in shape, suggesting a coordinated morphological adjustment to maintain swimming performance under acidified conditions. Quantification of the biomechanics and behavioral aspects of swimming improves predictions of larval survival and dispersal under present-day and future environmental conditions.

Sexual systems and life history of barnacles: A theoretical perspective

Abstract: Thoracican barnacles show one of the most diverse sexual systems in animals: hermaphroditism, dioecy (males and females), and androdioecy (males and hermaphrodites). In addition, when present, male barnacles are very small and are called "dwarf males". The diverse sexual systems and male dwarfism in this taxon have attracted both theoretical and empirical biologists. In this article, we review the theoretical studies on barnacles' sexual systems in the context of sex allocation and life history theories. We first introduce the sex allocation models by Charnov, especially in relation to the mating group size, and a new expansion of his models is also proposed. We then explain three studies by Yamaguchi et al., who have studied the interaction between sex allocation and life history in barnacles. These studies consistently showed that limited mating opportunity favors androdioecy and dioecy over hermaphroditism. In addition, other factors, such as rates of survival and availability of food, are also important. We discuss the importance of empirical studies testing these predictions and how empirical studies interact with theoretical constructs.

Dehydration and Drinking Responses in a Pelagic Sea Snake

Abstract: Synopsis Recent investigations of water balance in sea snakes demonstrated that amphibious sea kraits (Laticauda spp.) dehydrate in seawater and require fresh water to restore deficits in body water. Here, we report similar findings for Pelamis platurus, a viviparous, pelagic, entirely marine species of hydrophiine (‘‘true’’) sea snake. We sampled snakes at Golfo de Papagayo, Guanacaste, Costa Rica and demonstrated they do not drink seawater but fresh water at variable deficits of body water incurred by dehydration. The threshold dehydration at which snakes first drink fresh water is

Poecilogony and population genetic structure in Elysia pusilla (Heterobranchia: Sacoglossa), and reproductive data for five sacoglossans that express dimorphisms in larval development.

Abstract: Synopsis 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.

The Effects of Salinity on Acute Toxicity of Zinc to Two Euryhaline Species of Fish, Fundulus heteroclitus and Kryptolebias marmoratus

Abstract: It is well known that the toxicity of zinc (Zn) varies with water chemistry and that its bioavailability is controlled by ligand interactions and competing ions. Zn toxicity in freshwaters with varying water chemistry has been well characterized; however, far less attention has been paid to the toxicity of Zn in estuarine and marine systems. We performed experiments using two euryhaline species of killifish, Fundulus heteroclitus and Kryptolebias marmoratus, to investigate the effects of changing salinity on acute toxicity of Zn. Larvae (7- to 8-days old) of each species were exposed to various concentrations of Zn for 96 h at salinities ranging from 0 to 36 ppt and survival was monitored. As salinity increased, Zn toxicity decreased in both fish species, and at salinities above 10 ppt, K. marmoratus larvae were generally more sensitive to Zn than were those of F. heteroclitus. The protection of salinity against Zn toxicity in F. heteroclitus was further investigated to determine the role of Ca2+. Increased Ca2+ in freshwater protected against Zn toxicity to the same extent as did saline waters with an equal Ca2+ concentration up to ∼200 mg/L Ca for F. heteroclitus and ∼400 mg/L Ca for K. marmoratus. These results suggest that these two species may have differing Ca2+ requirements and/or rates of Ca2+ uptake in water of intermediate to full-strength salinity (∼200–400 mg/L Ca2+) and thus differ in their sensitivity to Zn. The overall goal of this study was to better understand Zn toxicity in waters of different salinity and to generate data on acute Zn toxicity from multiple species over a range of salinities, ultimately for use in development of estuarine and marine biotic ligand models.

Genetic and Morphological Differentiation of the Indo-West Pacific Intertidal Barnacle Chthamalus malayensis

Abstract: Chthamalus malayensis is a common intertidal acorn barnacle widely distributed in the Indo-West Pacific. Analysis of sequences of mitochondrial cytochrome c oxidase subunit I reveals four genetically differentiated clades with almost allopatric distribution in this region. The four clades exhibit morphological differences in arthropodal characters, including the number of conical spines and number of setules of the basal guard setae on the cirri. These characters are, however, highly variable within each clade; such that the absolute range of the number of conical spines and setules overlaps between clades, and therefore, these are not diagnostic characters for taxonomic identification. The geographic distribution of the four clades displays a strong relationship between surface temperatures of the sea and ocean-current realms. The Indo-Malay (IM) clade is widespread in the tropical, equatorial region, including the Indian Ocean, Malay Peninsula, and North Borneo. The South China (SC) and Taiwan (TW) clades are found in tropical to subtropical regions, with the former distributed along the coasts of southern China, Vietnam, Thailand, and the western Philippines under the influence of the South China Warm Current. The TW clade is endemic to Taiwan, while the Christmas Island (CI) clade is confined to CI. There was weak or no population subdivision observed within these clades, suggesting high gene flow within the range of the clades. The clades demonstrate clear signatures of recent demographic expansion that predated the Last Glacial Maximum (LGM), but they have maintained a relatively stable effective population in the past 100,000 years. The persistence of intertidal fauna through the LGM may, therefore, be a common biogeographic pattern. The lack of genetic subdivision in the IM clade across the Indian and Pacific Oceans may be attributed to recent expansion of ranges and the fact that a mutation-drift equilibrium has not been reached, or the relaxed habitat requirements of C. malayensis that facilitates high concurrent gene flow. Further studies are needed to determine between these alternative hypotheses.

Developmental causes of allometry: new models and implications for phenotypic plasticity and evolution.

Abstract: Shapes change during development because tissues, organs, and various anatomical features differ in onset, rate, and duration of growth. Allometry is the study of the consequences of differences in the growth of body parts on morphology, although the field of allometry has been surprisingly little concerned with understanding the causes of differential growth. The power-law equation y = ax(b), commonly used to describe allometries, is fundamentally an empirical equation whose biological foundation has been little studied. Huxley showed that the power-law equation can be derived if one assumes that body parts grow with exponential kinetics, for exactly the same amount of time. In life, however, the growth of body parts is almost always sigmoidal, and few, if any, grow for exactly the same amount of time during ontogeny. Here, we explore the shapes of allometries that result from real growth patterns and analyze them with new allometric equations derived from sigmoidal growth kinetics. We use an extensive ontogenetic dataset of the growth of internal organs in the rat from birth to adulthood, and show that they grow with Gompertz sigmoid kinetics. Gompertz growth parameters of body and internal organs accurately predict the shapes of their allometries, and that nonlinear regression on allometric data can accurately estimate the underlying kinetics of growth. We also use these data to discuss the developmental relationship between static and ontogenetic allometries. We show that small changes in growth kinetics can produce large and apparently qualitatively different allometries. Large evolutionary changes in allometry can be produced by small and simple changes in growth kinetics, and we show how understanding the development of traits can greatly simplify the interpretation of how they evolved.

Natural Selection, Larval Dispersal, and the Geography of Phenotype in the Sea

Abstract: Populations evolve generalist, specialist, and plastic strategies in response to environmental heterogeneity. Describing such within-species variation in phenotype and how it arises is central to understanding a variety of ecological and evolutionary topics. The literature on phenotypic differences among populations is highly biased; for every one article published on a marine species, at least 10 articles are published on a terrestrial species and eight focus on terrestrial plants. Here, I outline what we know from the marine literature about geographic variation in phenotype in the sea, with a principal focus on local adaptation. The theory of environmental "grain" predicts that the most likely evolutionary response (e.g., local adaptation, phenotypic plasticity, generalism, and balanced polymorphism) depends on the spatial scale of environmental variation relative to the distance that an organism disperses. Consistent with these predictions, phenotypic plasticity is stronger among invertebrates with geographically broad dispersal versus restricted dispersal (i.e., planktonic-dispersers versus direct-developers). However, contrary to predictions, the relative frequency, and spatial scale of local adaptation is not consistently greater among direct-developers relative to planktonic disperers. This indicates that the likelihood of local adaptation depends on other organismal or environmental traits. Two of the most vexing issues that remain include (1) predicting the extent to which barriers to dispersal are a cause versus consequence of phenotypic differentiation and (2) delineating the relative importance of evolutionary forces that favor or impede local adaptation. Understanding the mechanistic basis of the geography of phenotypic differences, or phenogeography, has gained recent momentum because of a need to predict impacts of global climatic change, anthropogenic disturbances, and dispersal of organisms to non-native habitats.