Integrating development and environment to model reproductive performance in natural populations of an intertidal gastropod

Functional challenges can differ among life-history stages,yet performance at one stage may be linked to the outcome ofperformance at others. For example, adult performance, in termsof the location or timing of reproduction in response to environmentalsignals, can set conditions that affect the performance of developmentalstages. In marine invertebrates, however, early performancehas been studied primarily in the laboratory. I outline an integrativeapproach to the study of field reproductive performance in amarine gastropod that undergoes development in intertidal habitats.Embryos within gelatinous masses experience high variabilityin development temperature and frequent exposure to thermalstress. In laboratory experiments, developmental performancewas measured as a function of maximum temperature (T_max) experiencedduring fluctuations that mimicked field tidal profiles. Performancecurves showed declines that coincided with temperature thresholdsfor heat shock protein (Hsp) expression, a signal of cellularstress. Application of laboratory results to field records ofT_max predicted large variation in the survival of embryos depositedon different days. Timing of field reproduction was non-randomwith respect to T_max, suggesting that adults could help to bufferembryos from environmental stress. Embryo survival, however,was not predicted to benefit from the non-random pattern ofadult reproduction. Adults may be constrained to respond toinformation that only weakly predicts conditions that embryoswill experience. Studies that incorporate linkages between lifecycle stages in the field may better reveal how performancecapacities and constraints at one stage can influence performanceand selection at others.     

Evolutionary approaches for studying functional morphology: examples from studies of performance capacity

Performance studies have long been a cornerstone of evolutionarystudies of adaptation because of their purported importancefor fitness. Nevertheless, for most systems, the mechanisticlink among habitat use, morphology and performance is poorlyunderstood. Further, few studies consider how behavior affectsthe relationship between morphology and performance. Here, Ihighlight the utility of considering both of these neglectedareas by discussing studies in two systems: (1) the evolutionof habitat use in Caribbean Anolis lizards, and (2) the evolutionof limb function in desert lizards. Caribbean Anolis lizardspartition the habitat via selection of different perch diameters,and surface diameter also exerts a strong effect on locomotorperformance. Phylogenetic analyses show that Anolis speciestend to avoid using perches in which their performance is submaximal,and also show that species with large performance breadths usea greater range of habitats. The underlying basis of this performanceto habitat use link is a trade-off between the ability to sprintquickly on broad surfaces and the ability to move effectivelyon narrow surfaces. Studies of the kinematics of high-speedlocomotion in five morphologically distinct lizard species revealthat some species exhibited behaviors that greatly enhancedtheir performance abilities relative to other species, suggestingthat behavior can play a key role in the link between morphologyand performance. Overall, these findings underscore the valueof using a mechanistic approach for studying the links betweenhabitat use, morphology and behavior.     

From odor molecules to plume tracking: an interdisciplinary, multilevel approach to olfaction in stomatopods

Like many marine crustaceans, mantis shrimp rely on their senseof smell to find food, mates, and habitat. In order for olfactionto function, odorant molecules in the surrounding fluid mustgain access to the animal's chemosensors. Thus fluid motionis important for olfaction, both in terms of the large scalefluid movements (currents, waves, etc.) that advect the odorantsto the vicinity of the sensors, and the small-scale viscositydominated flows that determine odorant access to the surfaceof the sensor. In order to understand how stomatopods interprettheir chemical environment, I investigated how stomatopod chemosensorymorphology and the movement of the structures bearing the chemosensorsaffect fluid access to the sensor surface in Gonodactylaceusmutatus. Preliminary results from new directions are presented,including mathematical modeling of molecular flux at the sensorsurface, field studies of the effects of ambient flow on odorsampling behavior, and flume experiments testing the abilityof stomatopods to trace odor plumes. Finally, I show how theuse of multiple techniques from several disciplines leads tonew ideas about the functional morphology of stomatopod antennules.     

Sources of Variation in Physiological Phenotypes and Their Evolutionary Significance

We offer the thesis that environmental physiologists and evolutionarybiologists can find fertile common ground in the study of howindividual variation in physiological phenotypes originatesand develops. The sources of such individual variation are oftencomplex; the consequences affect how natural selection willact on a suite of traits, of which some may seem, at first glance,far removed from the usual domain of environmental physiology.We illustrate our thesis in two ways. First, we offer two examplesdrawn from studies of thermal tolerance in the poeciliid fishHeterandria formosa. We show how fitness variation can be acomplex function of the gestational temperature and thermaltolerance and how these effects can produce environmentallyinduced variation among populations in thermal tolerance thatmimics a pattern of adaptive variation. Second, we review twocase studies that illuminate how environmental effects on amultivariate phenotype can channel the action of natural selection.The phenotypic plasticity of male life history in Poecilia latipinnain response to temperature embraces a spectrum of traits; theeffects of each one upon fitness will influence the abilityof selection to mold the response of any one of them to temperature.The phenotypic covariances in thermal tolerance and life-historytraits in Heterandria formosa differ slightly between populationsfrom different parts of the species range, apparently becauseof differences between them in thermal sensitivity; this differenceinsures that the multivariate nature of selection will be correspondinglydifferent in those different populations.     

Developmental stability and predation success in an insect predator-prey system

I investigated the relationships among developmental stability(as measured by individual bilateral asymmetry values), twomeasures of locomotory performance and predation success inan insect predator-prey system. In this system yellow dungfliesScathophaga stercoraria preyed upon houseflies Musca domesticainlaboratory-controlled conditions. There was no relationshipbetween locomotion and absolute asymmetry or mean size of twomorphological traits (fourth longitudinal wing vein, forelegtibia) in either species. Analysis of single predation trialsindicated that locomotion performance and trait size are notassociated with the probability of predation. However, Muscathat were captured had tibia that were more asymmetric thanMusca that survived. Similarly, Scathophaga that were successfulpredators had more symmetric forelegs than unsuccessful predators.There was no relationship between predation and wing vein asymmetry,which may indicate the importance of terrestrial-based predatoryavoidance tactics in this system. There were no relationshipsbetween morphology or locomotion with predation latency, preyhandling times, or the number of times a prey "escaped" froma predator. The mechanisms behind the relationship between tibiaasymmetry and predation success are discussed. This is the firstexperiment to reveal direct evidence for selection for symmetric,developmentally stable individuals through differential predation     

The Neural Network of the Limulus Retina: From Computer to Behavior

SYNOPSIS. The visual system of the horseshoe crab, Limulus polyphemus,provides an excellent opportunity for studying the neural basisof behavior. Quantitative analysis of the animal's visual behavioris now possible as is theoretical analysis of information processingin its retina. We combine these theoretical and behavioral approachesto investigate the nature of the signals the eye transmits tothe brain for the animal to see. Over the years theoretical studies of the Limulus eye were restrictedby the limited capabilities of single processor digital computers.However, a breakthrough in technology with the advent of parallelcomputers greatly enhances the analysis of large neural networkssuch as that of the retina. We have developed a time-dependentmodel of the Limulus retina on the Connection Machine (ModelCM-2), which is a massively parallel computer containing 32,768processors. The model represents a matrix of 64 x 128 receptorsand simulates interactions among receptors with digital filtersand transduction and adaptation within a receptor by a multistagecascade. Neural response patterns computed with the ConnectionMachine model replicate to a first approximation the patternsof neural activity recorded in the laboratory. Behavioral studies of Limulus vision carried out in the fieldcan be simulated on the Connection Machine. Neural responsesrecorded from behaving animals serve to test the accuracy ofthe model. Thus far we have developed just one model of theretina, but it eventually will have two forms, "daytime" and"nighttime," to account for the known circadian rhythms in retinalfunction. With a combination of field, physiological, and theoreticalstudies, we hope to gain a better understanding of the neuralmechanisms that underlie the animal's visually-guided behavior.     

STRONG ASSORTATIVE MATING BY DIET,COLOR, SIZE,AND MORPHOLOGY BUT LIMITED PROGRESS TOWARD SYMPATRIC SPECIATION IN A CLASSIC EXAMPLE: CAMEROON CRATER LAKE CICHLIDS

Models predict that sympatric speciation depends on restrictive parameter ranges, such as sufficiently strong disruptive selection and assortative mating, but compelling examples in nature have rarely been used to test these predictions. I measured the strength of assortative mating within a species complex of Tilapia in Lake Ejagham, Cameroon, a celebrated example of incipient sympatric adaptive radiation. This species complex is in the earliest stages of speciation: morphological and ecological divergence are incomplete, species differ primarily in breeding coloration, and introgression is common. I captured 27 mated pairs in situ and measured the diet, color, size, and morphology of each individual. I found strong assortative mating by color, size, head depth, and dietary source of benthic or pelagic prey along two independent dimensions of assortment. Thus, Ejagham Tilapia showed strong assortative mating most conducive to sympatric speciation. Nonetheless, in contrast to a morphologically bimodal Sarotherodon cichlid species pair in the lake, Ejagham Tilapia show more limited progress toward speciation, likely due to insufficient strength of disruptive selection on morphology estimated in a previous study (γ = 0.16). This supports the predicted dependence of sympatric speciation on strong assortment and strong disruptive selection by examining a potentially stalled example in nature.     

棉花叶片性状（厚度和油点密度）与其对绿盲蝽抗性的关系

为了明确棉花叶片性状（厚度和油点密度）与其对绿盲蝽Apolygus lucorum （Meyer-Dür）抗性的关系,以期为棉花抗盲蝽品种(系)选育提供理论依据,本研究选用对绿盲蝽有不同抗性的20个棉花品种(系)为材料,分别测定其叶片厚度、表皮层厚度和油点密度。结果表明：晋棉26、冀丰989、常D、亚洲棉对绿盲蝽表现为高抗;棉花叶片厚度、表皮层厚度和油点密度在不同生长期均有差异;棉花对绿盲蝽的综合抗性指数与其铃期叶片表皮层厚度和油点密度有显著相关性（y=20.673+0.415x,R²=0.305,P=0.012;y=1.049+0.049x,R²=0.207,P=0.044）。结果显示,在一定的生长期,叶片表皮层厚和多油点棉花品种可以减少绿盲蝽的危害。     

Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities

Ecologists and physiologists working on rocky shores have emphasizedthe effects of environmental stress on the distribution of intertidalorganisms. Although consumer stress models suggest that physicalextremes may often reduce predation and herbivory through negativeimpacts on the physiological performance of consumers, few fieldstudies have rigorously tested how environmental variation affectsfeeding rates. I review and analyze field experiments that quantifiedper capita feeding rates of a keystone predator, the sea starPisaster ochraceus, in relation to aerial heat stress, waveforces, and water temperature at three rocky intertidal siteson the Oregon coast. Predation rates during 14-day periods wereunrelated to aerial temperature, but decreased significantlywith decreasing water temperature. There was suggestive butinconclusive evidence that predation rates also declined withincreasing wave forces. Data-logger records suggested that thermalstress was rare in the wave-exposed habitats that I studied;sea star body temperatures likely reached warm levels (>24°C)on only 9 dates in 3 yr. In contrast, wind-driven upwellingregularly generated 3 to 5°C fluctuations in water temperature,and field and laboratory results suggest that such changes significantlyalter feeding rates of Pisaster. These physiological rate effects,near the center of an organism's thermal range, may not reducegrowth or fitness, and thus are distinct from the effects ofenvironmental stress. This study underscores the need to considerorganismal responses both under "normal" conditions, as wellas under extreme conditions. Examining both kinds of responsesis necessary to understand how different components of environmentalvariation regulate physiological performance and the strengthof species interactions in intertidal communities.     

Patterns of Parental Investment and Sexual Selection in Teleost Fishes: Do They Support Bateman's Principles?

Bateman demonstrated differences in variance for fertility andmating success between the sexes, with males usually havinga greater variance than females. Thus in general, male reproductivesuccess increases with number of mates acquired. These resultshave been referred to as "Bateman's principles" and taken togetherwith other parameters (e.g., relative parental investment) havebeen proposed to estimate a component of sexual selection. Forthis review I examine patterns of parental care and sexual selectionin teleost fishes (substrate brooding and with internal fertilization).I present data for the pumpkinseed sunfish Lepomis gibbosus,in which I estimated cost of paternal care and compared directmeasures of the intensity of selection on possible sexuallyselected traits to measures of sexual selection based on Bateman'sprinciples. Despite high levels of paternal care in substrate brooding fishes,sexual selection tends to act more strongly on males than onfemales, which suggests that maternal investment is higher thanpaternal investment and that parental care does not limit thereproductive rate for males. In pumpkinseed sunfish, selectionfavors parents with high levels of defense that may excludepredators more effectively and, as suggested by Bateman's measures,alternative reproductive strategies may decrease the opportunityfor sexual selection within the parental strategy. In teleostfishes with internal fertilization, patterns of parental investmentand intensity of sexual selection seem to support Bateman'sprinciples, but further studies using these systems and thesemeasures of selection will improve the understanding of factorsaffecting the intensity of sexual selection and its relationto mating systems.     

On the Ecology of Coexistence in Parthenogenetic and Bisexual Lizards of the Genus Cnemidophorus

In the center of their distribution in North America, membersof a complex of parthenogenetic and bisexual lizards of thegenus Cnemidophorus may be found side by side with one or moreof the others in a bewildering variety of patterns and ecologicalassociations. Exactly why so many congeneric species are foundliving together and exactly what their ecological, physiologicaland geographical requirements are remains virtually unknown.Here 1 summarize all reported cases of sympatry among six speciesof Cnemidophorus and discuss in detail specific examples ofsome of these interactions based on several years of field collectionsand observations. In addition I present the first field experimentalstudy designed to understand the ecological relationships ofsympatry in Cnemidophorus.     

Field observations of intraspecific agonistic behavior of two crayfish species,Orconectes rusticus and Orconectes virilis,in different habitats

Agonistic behavior is a fundamental aspect of ecological theories on resource acquisition and sexual selection. Crustaceans are exemplary models for agonistic behavior within the laboratory, but agonistic behavior in natural habitats is often neglected. Laboratory studies do not achieve the same ecological realism as field studies. In an attempt to connect laboratory results to field data and investigate how habitat structure affects agonistic interactions, the nocturnal behavior of two crayfish species was observed by scuba diving and snorkeling in two northern Michigan lakes. Intraspecific agonistic interactions were analyzed in three habitats: two food resources-macrophytes and detritus-and one sheltered habitat. The overall observations reinforce the concept that resources influence agonistic bouts. Fights in the presence of shelters were longer and more intense, suggesting that shelters have a higher perceived value than food resources. Fights in the presence of detritus patches had higher average intensities and ended with more tailflips away from an opponent, suggesting that detritus was a more valuable food resource than macrophytes. In addition, observations of aggressive behavior within a natural setting can add validity to laboratory studies. When fights in nature are compared with laboratory fights, those in nature are shorter, less intense, and less likely to end with a tailflip, but do show the fundamental fight dynamics associated with laboratory studies. Extrinsic and intrinsic factors affect intraspecific aggression in many ways, and both should always be recognized as having the potential to alter agonistic behavior.     

松褐天牛的交配行为

采用室内试验和野外观察相结合的方法,对松材线虫病的主要媒介昆虫松褐天牛Monochamus alternatus Hope的交配行为进行了研究。结果表明： 松褐天牛一次完整的交配包括相遇抱对、插入输精和配后保护3个阶段,在交配过程中雄虫有多次插入输精现象发生。室内试验中共观察到松褐天牛的交配123次,松褐天牛一次完整的交配过程平均需时63.49 min,其中输精前的抱对时间平均为1.68 min,交配过程中每次输精插入时间平均为57.60 s,配后保护时间为15.18 min。松褐天牛在开始交配的4天内平均交配5.15次,不同雄性个体所获得的交配机会差异很大。松褐天牛的交配行为表现出强烈的雄性竞争现象,雄虫能根据雌虫或自身的交配经历调整交配投入,当雌虫或者雄虫是初次交配时,总输精时间和插入输精的次数显著大于与有交配经历的雌虫或雄虫交配时的输精时间和插入输精次数。田间松褐天牛的交配行为与室内观察结果基本一致。     

Comparison of mouth morphology and prey size selection among three esocid taxa

Aquatic organisms, especially fishes, exhibit exceptional diversity in mouth morphology and this variation has been shown to influence foraging patterns. We compared mouth morphology among muskellunge Esox masquinongy, northern pike Esox lucius and their hybrid, tiger muskellunge E. masquinongy x E. lucius. Head and mouth size among the three taxa were similar for juveniles (<400 mm total length), but diverged with increasing length, being greater for northern pike than muskellunge. Tiger muskellunge had a head and mouth size intermediate to the two, but more similar to northern pike than muskellunge. Morphological differences among taxa were related to data examining prey size selection in laboratory and field experiments. In the laboratory, northern pike selected prey that were smaller than their maximum mouth width (widest point between outside corners of mouth), tiger muskellunge selected larger prey, and muskellunge size-selection was intermediate between the other two taxa. Among the three esocids, muskellunge had the smallest increase in handling time with increasing prey body depth relative to predator mouth width. In a common garden field experiment in three lakes containing mainly deep-bodied prey, results generally followed morphological patterns, with northern pike selecting larger prey compared to muskellunge. Although morphology predicted most of the variation in greatest body depth of prey consumed, the best predictor of prey size was a model that included predator mouth width, taxon, and interaction. Information comparing prey size selection among esocid taxa is useful for understanding how to manage esocid populations based on system-specific prey characteristics and also for understanding how variations in morphological characteristics of apex predators can influence prey vulnerability and ecosystem structure.     

Adaptive evolution of butterfly wing shape: from morphology to behaviour

Butterflies display extreme variation in wing shape associated with tremendous ecological diversity. Disentangling the role of neutral versus adaptive processes in wing shape diversification remains a challenge for evolutionary biologists. Ascertaining how natural selection influences wing shape evolution requires both functional studies linking morphology to flight performance, and ecological investigations linking performance in the wild with fitness. However, direct links between morphological variation and fitness have rarely been established. The functional morphology of butterfly flight has been investigated but selective forces acting on flight behaviour and associated wing shape have received less attention. Here, we attempt to estimate the ecological relevance of morpho‐functional links established through biomechanical studies in order to understand the evolution of butterfly wing morphology. We survey the evidence for natural and sexual selection driving wing shape evolution in butterflies, and discuss how our functional knowledge may allow identification of the selective forces involved, at both the macro‐ and micro‐evolutionary scales. Our review shows that although correlations between wing shape variation and ecological factors have been established at the macro‐evolutionary level, the underlying selective pressures often remain unclear. We identify the need to investigate flight behaviour in relevant ecological contexts to detect variation in fitness‐related traits. Identifying the selective regime then should guide experimental studies towards the relevant estimates of flight performance. Habitat, predators and sex‐specific behaviours are likely to be major selective forces acting on wing shape evolution in butterflies. Some striking cases of morphological divergence driven by contrasting ecology involve both wing and body morphology, indicating that their interactions should be included in future studies investigating co‐evolution between morphology and flight behaviour.     

Physiological community ecology: variation in metabolic activity of ecologically important rocky intertidal invertebrates along environmental gradients

Rocky intertidal invertebrates live in heterogeneous habitatscharacterized by steep gradients in wave activity, tidal flux,temperature, food quality and food availability. These environmentalfactors impact metabolic activity via changes in energy inputand stress-induced alteration of energetic demands. For keystonespecies, small environmentally induced shifts in metabolic activitymay lead to disproportionately large impacts on community structurevia changes in growth or survival of these key species. Herewe use biochemical indicators to assess how natural differencesin wave exposure, temperature and food availability may affectmetabolic activity of mussels, barnacles, whelks and sea starsliving at rocky intertidal sites with different physical andoceanographic characteristics. We show that oxygen consumptionrate is correlated with the activity of key metabolic enzymes(e.g., citrate synthase and malate dehydrogenase) for some intertidalspecies, and concentrations of these enzymes in certain tissuesare lower for starved individuals than for those that are wellfed. We also show that the ratio of RNA to DNA (an index ofprotein synthetic capacity) is highly variable in nature andcorrelates with short-term changes in food availability. Wealso observed striking patterns in enzyme activity and RNA/DNAin nature, which are related to differences in rocky intertidalcommunity structure. Differences among species and habitatsare most pronounced in summer and are linked to high nearshoreproductivity at sites favored by suspension feeders and to exposureto stressful low-tide air temperatures in areas of low wavesplash. These studies illustrate the great promise of usingbiochemical indicators to test ecological models, which predictchanges in community structure along environmental gradients.Our results also suggest that biochemical indices must be carefullyvalidated with laboratory studies, so that the indicator selectedis likely to respond to the environmental variables of interest.     

Locomotor compensation creates a mismatch between laboratory and field estimates of escape speed in lizards: a cautionary tale for performance-to-fitness studies

A key assumption in evolutionary studies of locomotor adaptation is that standard laboratory measures of performance accurately reflect what animals do under natural circumstances. One widely examined measure of performance is maximum sprint speed, which is believed to be important for eluding predators, capturing prey, and defending territories. Previous studies linking maximum sprint speed to fitness have focused on laboratory measurements, and we suggest that such analyses may be appropriate for some species and intraspecific classes, but not others. We provide evidence for a general inverse relationship between maximum laboratory sprint speed and the percentage of maximum capacity that animals use when escaping from a threat in the field (the model of locomotor compensation). Further, absolute values of field escape speed and maximum laboratory speed are not significantly related when comparing across a diverse group of Anolis and lacertid lizards. We show that this pattern of locomotor compensation holds both within (i.e., among intraspecific classes) and among lizard species (with some exceptions). We propose a simple method of plotting field escape speed (y-axis) versus maximum laboratory speed (x-axis) among species and/or intraspecific classes that allows researchers to determine whether their study organisms are good candidates for relating laboratory performance to fitness. We suggest that species that reside directly on, or near the "best fitness line" (field escape speed = maximum laboratory speed) are most likely to bear fruit for such studies.     

Interactive effects of sex and temperature on locomotion in reptiles

Males and females from several animal taxa differ in locomotorperformance traits such as sprinting and jumping. These performancedimorphisms may be explained at least partially by sexual differencesin physiology or morphology. In ectotherms such as reptiles,however, thermal ecology places an additional constraint onrealized locomotor performance. I review recent studies on reptilesexamining sexual differences in locomotor capacity and relatedthermoregulatory behavior, and discuss potential causes, constraints,and selective pressures that might drive intersexual divergencein capacity for locomotor performance in reptiles. In severalcases where such differences occur, sexual dimorphisms in bodysize do not account for all the observed variation in performance.However, while sex-specific locomotor capacities might be evidentin the laboratory, ecological performance in nature is likelythe result of complex interactions among sex, thermal sensitivity,habitat type, and behavioral locomotor compensation. Resultsfrom laboratory studies of dimorphisms in maximum locomotorcapacity are therefore likely to be poor predictors of realizedecological differences in performance. Nonetheless, sex differencesin performance are potentially important modifiers of male andfemale behavioral strategies and overall fitness, and consequentlyare deserving of more attention than they have thus far received.     

Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the system of mating

Early field work on naked mole-rats, Heterocephalus glaber, suggestedthat small colonies are rare and that colonies can only formby fissioning of existing colonies. Many researchers expectedthat this would result in extreme inbreeding and high relatednesswithin colonies and would thus explain the evolution of eusocialityin naked mole-rats. Here I report evidence of dispersers andoutbreeding in colonies of wild naked mole-rats that suggeststhat inbreeding is not the system of mating for this speciesand that outbreeding is probably frequent. Wild dispersers havethe same morphology as was reported for dispersers in laboratorycolonies. Low levels of genetic variation in previous moleculargenetic studies of naked mole-rats probably result from theviscous population structure typical of fossorial rodents.     

Environmental variation and selection on performance curves

Many aspects of physiological and organismal performance varywith some continuous environmental variable: e.g., photosyntheticrate as a function of light intensity; growth rate or sprintspeed as a function of temperature. For such ‘performancecurves’, the environment plays two roles: it affects boththe levels of performance expressed, and the relationship betweenperformance and fitness. How does environmental variation withina generation determine natural selection on performance curves?We describe an approach to this question that has three components.First, we quantify natural environmental variation and assessits impact on performance in the field. Second, we develop asimple theoretical model that predicts how fine-grained environmentalvariation determines selection on performance curves. Third,we describe how directional selection on performance curvesmay be estimated and compared to theoretical predictions. Weillustrate these steps using data on performance curves of short-termgrowth rate as a function of temperature (thermal performancecurves) in Pieris caterpillars. We use this approach to explorewhether selection acts primarily on growth rate at specifictemperatures, or on more integrated aspects of growth.