Historical and ecological correlates of body shape in the brook stickleback, Culaea inconstans

Using geometric morphometric methods, we evaluated the correlation between phenotypic variation and available historical and habitat information for two genetically differentiated, allopatric lineages of a widespread North American species, the brook stickleback ( Culaea inconstans ). The results obtained revealed strong patterns of structured phenotypic differentiation across the species range with extreme phenotypes occurring at the northwest and southeast range boundaries. Shape variation was broadly congruent with the distribution of two mitochondrial DNA lineages; a deep-bodied eastern form (Atlantic refugium) and a slim-bodied western form (Mississippian refugium); however, the two forms were not lineage-specific and phenotypic cladistic diversification is likely to be an artefact of underlying clinal variation associated with longitudinal and latitudinal gradients. In addition, we found little evidence of diagnosable lake and river forms across North America. Taken together, large-scale patterns of phenotypic diversity observed in C. inconstans suggest that relatively recent factors, such as continually varying natural selection across the range and/or potential local gene flow, may substantially mitigate the effects of historical separation or a generalized adaptive response to alternative habitats.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 769–783.     

Assemblage and population-level consequences of forest fragmentation on bilateral asymmetry in tropical montane birds

Habitat fragmentation has the potential to influence the development and thus the phenotype of organisms. The asymmetry of bilateral traits may be indicative of the extent to which developmental stability is compromised by the stressful conditions underlying fragmentation. Using an assemblage- and population-level approach, we explored asymmetry differences in tarsus and outermost tail feathers of birds inhabiting fragmented landscapes in the tropical Andes of Colombia. More than 2500 individuals of 185 species were mist-netted at nine forest sites representing continuous forest (> 1000 ha), medium- (70–110 ha), and small-sized (8–20 ha) fragments. Feathers showed true fluctuating asymmetry (FA), whereas tarsus presented a mixture of FA and directional asymmetry. Overall, asymmetry was lowest in continuous forest, and highest in small and medium fragments. These patterns remained unchanged when directionality and differences in species composition, abundance, and foraging tactics were considered. The population-level analyses showed a general trend of increased asymmetry variation in fragments, yet the responses were not always in the same direction. Increased asymmetry may represent an outcome of processes that contribute to the persistence of species in changing environments, and to the generation of phenotypic innovation, which suggests individual adjustments of development to deal with stress. This calls into question the deliberated application of FA as a biomonitoring tool for conservation.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 119–133.     

Repeatability of size and fluctuating asymmetry of antler characteristics in red deer (Cervus elaphus) during ontogeny

Fluctuating asymmetry (FA) has been suggested as a measure of the sensitivity of development to a wide array of genetic and environmental stresses. It has been also suggested that antlers in red deer could be important during social and rutting displays. We used antler measurements of 51 males that were measured over subsequent seasons, from 3–8 years of age, and analysed three antler traits: antler weight, length, and the number of antler tines (antler size). We calculated absolute and relative FA. All three size traits were highly significantly intercorrelated. By contrast to this, the FA of the three traits, did not show such relationships. With increasing age, antler size and FA also increased. When testing the repeatability of FA and antler size, there was a principal difference in the pattern between FA and antler size, with the latter being much more consistent than the former. This suggests that antler size, not FA, may be a good predictor of the bearer's quality in mate selection. This fits well with the good-genes hypothesis that the development of extravagant secondary sexual characters can be an honest advertisement of heritable male quality.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 215–226.     

Geographical variation in asymmetry in Gasterosteus aculeatus

We tested whether fluctuating asymmetry (FA) in undisturbed populations is associated with several natural environmental factors and whether FA is negatively correlated with fitness in the wild. We compared the FA of multiple bony structural defences among 87 endemic populations of threespine stickleback ( Gasterosteus aculeatus L.) inhabiting pristine freshwater habitats on the islands of Haida Gwaii, British Columbia, Canada. Multi-trait FA for adults and juvenile fish varied extensively among populations, but only in adults did it correlate with geography and two habitat characteristics (pH and water colour). Mean FA among individual traits varied concordantly among populations but was not correlated within individuals. While asymmetrical fish showed slightly higher levels of parasitism as predicted, selection differentials based on age class comparisons suggested that asymmetrical fish had the same or marginally higher survival than symmetrical fish. Selection differentials of FA varied significantly among traits and may reflect variability in their functional importance and in the strength of selection on their developmental stability. The data imply that FA/fitness associations are heterogeneous and character-specific.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 9–22.     

Stable isotopic niche predicts fitness of prey in a wolf–deer system

Interindividual variation in niche presents a potentially central object on which natural selection can act. This may have important evolutionary implications because habitat use governs a suite of selective forces encountered by foragers. In a free-living native black-tailed deer, Odocoileus hemionus , population from coastal British Columbia, we used stable isotope analysis to identify individual variation in foraging niche and investigated its relationship to fitness. Using an intragenerational comparison of surviving and nonsurviving O. hemionus over 2 years of predation by wolves, Canis lupus, we detected resource-specific fitness. Individuals with isotopic signatures that suggested they foraged primarily in cedar ( Thuja plicata )-dominated and low-elevation hemlock ( Tsuga heterophylla )-dominated forest stands were more likely to be killed by C. lupus . High-quality forage in T. plicata stands, as indexed by protein content, may be involved in maintaining this foraging phenotype. Moreover, nonsurvivors diverged more than survivors from median isotopic signatures, suggesting selection against foraging specialization. Stable isotope analysis provides a novel opportunity to integrate ecological and selective landscapes in order to identify underlying ecological mechanisms of selection and provide insight into the maintenance of variability.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 125–137.     

Asymmetric female genitalia and other remarkable morphology in a new genus of cobweb spiders (Theridiidae, Araneae) from Madagascar

Symmetry is such a conspicuous feature of life that asymmetries draw our immediate attention. While not uncommon in bilateral organisms in general, asymmetry in spiders is rare. Here I report the first case of antisymmetry in external female genitalia in spiders, in the new genus Asygyna (Theridiidae: Araneae) from Madagascar. In the nearly 39 000 species of spiders described to date, the external structure of the female genitalia is symmetric. In entelegyne spiders paired external copulatory openings each lead to an internal copulatory duct, whose roughly symmetrical trajectories terminate in paired receptacles, the spermathecae. In Asygyna , here exemplified by two new species, A. huberi and A. coddingtoni , laterality is evident in the internal and external female genitalia. A single copulatory opening leads (either to the left or right depending on the individual) to a single copulatory duct with a distinctly asymmetric trajectory. The duct splits terminally shortly before entering the two spermathecae. The males are symmetric, but possibly only one palp can be used in copulation with each female. If adaptive, the selective forces behind this asymmetry are perplexing, as male access to females seems reduced. However, if males are plentiful, asymmetry may benefit the female by reducing insertion times and thus shortening copulation time, and by tightening her control over which males sire her offspring. Asygyna has a range of other bizarre sex-related morphologies, including prosomal pits and a well developed stridulatory mechanism in both sexes, a male proboscis, and simplified palps. A phylogenetic analysis, including 63 taxa and 242 morphological characters, places Asygyna in Pholcommatinae, sister to the enigmatic genus Carniella .  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 211–232.     

Geographical and Temporal FA Variation in Threespine Stickleback Populations from Galicia (NW Spain)

Subtle departures from bilateral symmetry (FA) in morphological traits has been used as a measure of developmental stability in populations subjected to genetic and environmental processes as inbreeding, pollution or parasitic infection. Geographic variation of FA was assessed in 19 threespine stickleback (Gasterosteus aculeatus) populations from Miño and Limia rivers, from Galicia (NW Spain). This variation was evaluated using four FA indices on five meristic and one morphometric traits. Temporal variation of FA was also assessed using several samples through time in only one population. Significant geographical variation was detected for pectoral fin rays, lateral forks, lateral plates and spine length. Lateral plates, upper gillrakers, pectoral fin rays and spine length showed significant variation through the time. The variation of FA through the time showed a common performance for all characters during the period considered: a slight increase in the intermediate months with a decrease at the end of the period. Symmetric and asymmetric sticklebacks exhibited similar infection, with one exception: symmetric sticklebacks for lower gillrakers of Antela populations exhibited increased parasite infection relative to asymmetric ones. Sticklebacks with extreme phenotypes exhibited much higher levels of asymmetry than modal ones in all samples for all traits.     

Macro-alga population shows low but significant heterogeneity in developmental instability with no detectable association with individual fitness

We studied among-individual variation in developmental instability (DI) and fitness-related parameters in 80 individual plants of Fucus vesiculosus (Phaeophyta). To minimize differential environmental effects, plants were sampled from one environmentally homogenous population. DI was measured as fluctuating asymmetry (FA) of four bilaterally symmetric traits (branch length, receptacle length and width, and bladder width) for an average total of 30 structures per individual. FA levels varied significantly among individual plants, consistent with a coefficient of variation of 0.12 for organism-wide DI or 0.13–0.21 for trait-specific DI. These values are lower than estimates for other organisms, suggesting that the genetic heterogeneity in DI was low. The data provide some evidence for organism-wide DI, but simulations show that organism-wide and trait-specific variation cannot be conclusively separated. Growth rate of branch tips was determined experimentally, demonstrating significant variation among individuals. FA was not significantly correlated with growth rate or with morphological variables associated with fecundity, age, size, and health. At the same time, the signs of all the correlation coefficients were consistent with the expectation of a negative relationship between DI and fitness. The simulations indicated that the correlation between FA and the underlying DI was comparatively strong (high hypothetical repeatability), implying that the lack of significant associations between FA and fitness variables reflected a weak relationship between DI and these fitness parameters. This weak relationship may be related to the low amount of DI variation in the study population.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 277–286.     

Procrustean analysis of fluctuating asymmetry in the bulb mite Rhizoglyphus robini Claparede (Astigmata: Acaridae)

We studied fluctuating asymmetry (FA) in two generations of the bulb mite Rhizoglyphus robini . We used Procrustes analyses, which allow the comparison of dimensionless shapes of body sides. We found little (<4%) directional asymmetry in either sex. Of the two morphs occurring in this species, fighters, which possess a thickened third pair of legs, exhibited higher FA than did scramblers, the morph with unmodified legs; this may reflect the costliness of the fighter developmental pathway. There was a negative relationship between FA and female fecundity, but the regression slope of mid-offspring on mid-parent FA was not significantly greater than zero. We propose that heritability estimates can be biased downwards if highly asymmetric individuals produce fewer viable offspring. However, we found no significant association between parental FA and the proportion of viable embryos in their broods. Furthermore, we hypothesized that parental FA might indicate the presence of largely recessive mutations deleterious to developmental homeostasis that would cause increased embryo mortality under inbreeding. However, we found no significant association between FA of parents that were mated to their full sibs and the proportion of viable embryos in their inbred progeny.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 499–505.     

Pectoral fin size in a fish species with paternal care: a condition-dependent sexual trait revealing infection status

1. The three-spined stickleback, Gasterosteus aculeatus L., is a territorial fish with exclusive male parental care. Males oxygenate the eggs with fanning movements of their pectoral fins. The present authors investigated whether the apparent sexual differences in the functional demands of the pectoral fins have resulted in sexual differences in fin size. If males have relatively larger pectoral fins, females may use this as a signal to aid their mate choice for good fathers. Therefore, further objectives were to study the condition-dependency of relative pectoral fin size in males and the relationship with male parasite load. 2. Reproductively active males possessed relatively larger pectoral fins than females in both wild-caught and laboratory-bred fish. 3. In the field, caring males with relatively large pectoral fins were in better physical condition and had more food in their stomachs. 4. Relatively small pectoral fins and poor body condition were associated with infection by the intestinal parasite Pomphorhynchus laevis (Acanthocephala), the prevalent parasite species in the study population.     

Hybridization between two polyphagous fruit-fly species (Diptera: Tephritidae) causes sex-biased reduction in developmental stability

When hybridization modifies the genetic constitution of individuals or populations, the stability of phenotypic development may either decrease or increase, depending on the divergence in the gene systems that control the development between the hybridizing taxa, i.e. on the relative effects of outbreeding and heterosis. In genetically closely related species, strong heterotic effects are less likely to occur, and hence hybridization may be expected to cause an overall decrease in developmental stability (DS) resulting from the disruption of coadapted gene complexes. To test this hypothesis, we experimentally crossed two closely related species of Ceratitis fruit flies and compared multiple-trait fluctuating asymmetry (FA, a measure of DS) in male and female offspring between parental species and two crossbred types. All traits measured play an important role in the fanning and buzzing behaviour associated with male courtship in Ceratitis , or are located on body parts involved in this behaviour. As predicted, hybrid offspring developed more asymmetrically than offspring of either parental species – most notably in meristic traits – and the increase in FA was consistently and significantly stronger in females than in males. The fact that males buffered their development more efficiently than females is in concordance with the presumed between-sex variation in functionality, and hence cost of asymmetry, of the measured traits. Absence of a similar sex difference in DS among parental offspring is believed to result from overall weak association between DS and FA in the absence of genetic stress, resulting from the random nature of the underlying processes that trigger asymmetric development.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 579–588.     

Morphological asymmetry of insular freshwater populations of threespine stickleback

Fluctuating asymmetry (FA), random deviations from perfect symmetry in a bilateral organism, has been widely used as a proxy for developmental instability in stressed populations. In order to test the utility of FA of resident freshwater threespine stickleback (Gasterosteus aculeatus) as a biomonitoring tool for contaminated sites, we compared levels of asymmetry of seven morphological traits of threespine stickleback collected from lakes at three islands with a history of military contamination and three islands with no military history, in the Aleutian Archipelago, Alaska. Traits examined include eye diameter, operculum width, pectoral fin ray number, pectoral fin width, lateral plate number, lateral plate length, and pelvic spine length. All morphometric traits demonstrated some degree of FA or directional asymmetry (DA), but the military history of a lake was not a predictor of the degree or type of asymmetry. Overall, the patterns of asymmetry were similar for all traits, irrespective of military contamination at a lake. Our results demonstrate that the suite of threespine stickleback traits measured are not suitable for examination of FA as a proxy for aquatic pollution in this region. DA also does not appear to be suitable as an indicator of aquatic pollution, but may instead be driven by local ecological factors such as predation.     

Evidence for asymmetric migration load in a pair of ecologically divergent stickleback populations

Gene flow between ecologically divergent populations can prevent local adaptation, resulting in lower mean fitness and directional selection within a population. Such maladaptation should tend to be stronger in populations receiving a relatively larger fraction of immigrants. We test this expectation by comparing the strength of selection in a pair of three-spine stickleback populations in adjoining but unequal-sized lake basins in British Columbia. A larger deeper basin is connected to a smaller shallower basin by a short channel that allows extensive migration between populations. The two basins contain distinct habitats and prey communities, and stickleback stomach contents and isotope ratios differ accordingly. Trophic morphology is correlated with diet, so we would expect these ecological differences to be accompanied by morphological divergence. However, high gene flow appears to constrain adaptive divergence: microsatellites indicate that the two basins represent a single panmictic gene pool, and phenotypic divergence is very subtle. As a result, fish in the smaller lake basin are subject to persistent directional selection towards a more benthic phenotype, whereas the larger population exhibits no significant selection. The results illustrate the potentially asymmetrical effect of migration-selection balance, and its effect on fitness within populations.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 273–287.     

Heterospecific aggression and adaptive divergence in brook stickleback (Culaea inconstans)

Agonistic behavior between heterospecifics, in which individuals of one species attack another, may cause a subordinate species to shift resource or habitat use. Subsequent evolutionary responses to selection may mimic shifts expected under ecological character displacement, but with no role played by exploitative competition. Alternatively, aggressive behavior can evolve when fitness is improved by excluding members of a coexisting species from a defendable resource through interference. We tested whether heterospecific agonistic behavior has evolved in brook stickleback (Culaea inconstans) by comparing replicate allopatric populations to those sympatric with ninespine stickleback (Pungitius pungitius). We also tested for heritable variation in heterospecific aggressive behavior by rearing family groups in a common environment. Allopatric populations of brook stickleback were more aggressive than ninespine stickleback, suggesting that pre-existing aggression in brook stickleback contributed to niche shifts by ninespine stickleback. In addition, sympatric adult brook stickleback were more aggressive toward ninespine stickleback than brook stickleback from allopatric populations. Overt heterospecific aggressive behaviors were heritable, and aggression in juvenile brook stickleback increased with age in sympatric but not in allopatric populations reared in a common environment. Brook stickleback have evolved increased aggression when they coexist with ninespine stickleback. These stickleback communities have been structured by both evolved and pre-existing variation in heterospecific aggressive behavior in brook stickleback.     

Sexual selection for symmetrical male medflies (Diptera: Tephritidae) confirmed in the field

The role of fluctuating asymmetry as an indicator of fitness to females in mate choice remains controversial. Previous studies indicated that male medflies with symmetrical supra-fronto-orbital (SFO) bristles achieve relatively high mating success under laboratory conditions. Here we present data from field cage studies of wild collected medflies in Guatemala and Crete, which reveal the same association between fluctuating asymmetry in SFO bristle length and mating success as that seen in the laboratory. The experiments in Crete included males that were missing one or both of their bristles. A comparison of mating success between the three groups indicated that the mere presence of bristles did not exert a major influence. Analysis of attempted courtships suggests that the association between male mating success and FA in bristle length appears to be generated as a result of females being more likely to enter into courtships with symmetrical males, rather than through a rejection of asymmetrical males during or after it. This raises the possibility that the primary stimulus that makes a symmetrical male attractive is acting at too great a distance to depend on symmetry itself. Alternatives might include superior pheromone emissions or the occupation of a prime location within the lek.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81 , 347–355.     

Asymmetry and fitness in female yellow dung flies

Fluctuating asymmetry (FA) has been widely used as a measure of developmental stability, and two recent meta-analyses suggest FA may be associated with several fitness components, including fecundity, growth rate and longevity. However, these studies have been strongly criticised on a number of grounds, and it was suggested that further evidence was required before the importance of any associations could be accurately assessed. Furthermore, studies should be of individual FA and fitness components. Here we investigated associations between individual FA of the mid and hind tibia and several fitness related traits (including fecundity, fertility, longevity and offspring development time) in female yellow dung flies ( Scathophaga stercoraria ). As in several previous studies, asymmetry could be discerned from measurement error and was FA. However, we found no significant associations between any measure of FA and any fitness component regardless of how the data were analysed. Our results therefore do not support any fitness–FA association and suggest that as with other aspects of FA, associations may be trait and species specific.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 557–563.     

Fluctuating asymmetry in bank vole populations (Rodentia, Arvicolinae) reflects stress caused by landscape fragmentation in the Mont-Saint-Michel Bay

In intensively farmed, reclaimed areas (polders) of Mont-St-Michel Bay, France, bank voles ( Clethrionomys glareolus ) live in fragmented hedgerows, where populations are small and dispersal rates and genetic diversity are low. These small populations are likely to have been exposed to potential environmental and/or genetic stress. The sensitivity of development to stress can be measured by fluctuating asymmetry (FA). FA was calculated for three samples from a disturbed area and one sample from an adjacent, more connected and undisturbed landscape. Size FA was estimated from 16 measurements of the skull and teeth whilst shape asymmetry was estimated from the skull alone. Bank voles in fragmented hedgerows of the disturbed area had a higher degree of FA than bank voles from the more extensive and more connected hedges of the undisturbed area. These results were confirmed by the study of shape asymmetry, body mass and centroid size of the skull. There were no differences in FA between the three disturbed area samples. We conclude that FA does not reveal differences in the development of bank voles living in isolation under different local conditions in the various parts of the disturbed area. However, FA may allow differentiation between populations from greatly contrasting landscapes.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80, 37–44.     

Fitness, developmental instability, and the ontogeny of fluctuating asymmetry in Daphnia magna

Fluctuating asymmetry (FA) is the most commonly used measure of developmental instability. The relation between FA and individual fitness remains controversial, partly due to limited knowledge on the mechanisms behind variation in FA. To address this, we investigated the associations between FA, growth and reproduction as well as the ontogeny of FA in a clonal population of Daphnia magna . FA was not correlated with growth and reproduction, either at the between- or the within-individual level, in a high ( N  = 48 individuals) or in a low ( N  = 52 individuals) food-quantity regime. There were therefore no indications of functional effects of FA or of phenotypic trade-offs between developmental stability, growth and reproduction. Individual asymmetries varied randomly in sign and magnitude between subsequent molts ( N  = 19 individuals, 9–11 instars), but the levels of FA were generally lowest at intermediate ages. No feedback between right and left sides was detected. This suggests that FA only reflects the most recent growth history, that developmental instability may increase in old age, and that FA depends on processes operating on each side of the body independently. The results also suggest that FA differences within and among individual Daphnia are largely random, with limited biological significance.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 179–192.     

The relationship between skull morphology, biting performance and foraging mode in Kalahari lacertid lizards

Lizards are a diverse clade in which one radiation consists entirely of sit-and-wait foragers and another consists of wide foragers. Lizards utilizing these two foraging modes are known to differ in diet, but little is known about how feeding morphology relates to diet and/or foraging mode. This study tested the hypothesis that skull morphology and biting performance are related to diet preference, and consequently, coevolve with foraging mode. Four species of lacertid lizard were studied because they vary in foraging mode, their phylogenetic relationships are known and they are well studied ecologically. Using an 'ecomorphological' approach, skull morphology and biting performance were quantified and mapped on to the phylogeny for the species. The results indicate that sit-and-wait species have shorter, wider skulls than the wide foraging species, and that all are significantly different in overall head shape. The sit-and-wait species had similar values for biting performance; however, clear phylogenetic patterns of covariation were not present between sit-and-wait and wide foraging species for either biting performance or skull morphology. Thus, skull morphology and performance have little influence on diet and foraging mode in these species. Instead it is likely that other factors such as seasonal prey availability and/or life history strategy shape foraging mode decisions.  © 2004 The Linnean Society of London, Zoological Journal of the Linnean Society , 2004, 140 , 403–416.     

Learned Recognition of Heterospecific Alarm Signals: The Importance of a Mixed Predator Diet

A wide diversity of aquatic organisms release alarm signals upon being attacked by a predator. Alarm signals may 'warn' nearby individuals of danger. Moreover, the signals may be important in facilitating learned recognition of unknown stimuli. It is common for different prey species to respond to each other's chemical alarm signals. In many cases, the responses are learned but no learning mechanisms have been identified to date. In this study we tested whether prey fish can learn the identity of an unknown alarm signal when they detect it in association with conspecific alarm cues in the diet of a predator. Chemical alarm cues are known to be conserved in the diet of predators. We conditioned fathead minnows ( Pimephales promelas ) with chemical stimuli from predatory yellow perch ( Perca flavescens ) fed a mixed diet of minnows and brook stickleback ( Culaea inconstans ), perch fed a mixed diet of swordtails ( Xiphophorus helleri ) and stickleback or distilled water. Minnows were subsequently exposed to chemical alarm cues of injured stickleback alone. Those minnows previously conditioned with perch fed a mixed diet of minnows and stickleback increased their use of shelter and 'froze' significantly more than minnows previously conditioned with perch fed a diet of swordtails and stickleback or those exposed to distilled water. These data demonstrate a mechanism by which minnows can learn the identity of a heterospecific alarm signal.