Long-term variation in colour-morph frequencies in the spider Enoplognatha ovata (Glerck) (Araneae: Theridiidae): natural selection, migration and intermittent drift

The spider Enoplognatha ovata is univoltine. It has three principal visible morphs, lineata, redimita and mala , whose genetics are understood. Phenotype frequencies and population sizes have been estimated at 44 sites in a single valley in Yorkshire for periods of up to 15 years. Geographically, recognizable areas of high and low frequencies of redimita and ovata are found, typically a few hundred metres across. Statistically significant frequency differences also exist on a scale of tens of metres between adjacent sites. Temporal variation in lineata allele frequency has been investigated using a weighted regression technique assuming either no deterministic change or a steady change at constant rate. There is little direct evidence for selection but variation within sites is less than would be expected through genetic drift. A negative relationship is demonstrated between initial allele frequency in a site and the direction and rate of allele frequency change with time, suggesting that populations are moving towards a global equilibrium. This conclusion is insensitive to varying assumptions about the relationship between estimated and effective population sizes. Evidence from transplantation experiments and from the most isolated site indicate that both migration and selection contribute to this trend. We suggest that populations were stochastically perturbed from the equilibrium during bottlenecks in population size which resulted from major habitat disturbance about 35 years ago.     

Spatial variation in colour morph, spotting and allozyme frequencies in the candy-stripe spider, Enoplognatha ovata (Theridiidae) on two Swedish archipelagos

The selective significance, if any, of many invertebrate visible polymorphisms is still not fully understood. Here we examine colour- and black spotting-morph frequencies in the spider Enoplognatha ovata in populations on two Swedish archipelagos with respect to different spatial scales and, in one archipelago, against the background of variation at four putative neutral allozyme marker loci. Every population studied was polymorphic for colour and 28 out of 30 contained all three colour morphs – lineata, redimita and ovata. We found no evidence for a breakdown in the traditional colour morph designation previously suggested for other northern European populations of this species. For colour there is no significant heterogeneity at spatial scales greater than between local populations within islands. Black spotting frequencies show a similar lack of pattern over larger spatial scales except that there are significant differences between the Stockholm and Göteborg archipelagos. Measures of population differentiation (θ) within the Stockholm islands for the two visible systems show them to be significantly more differentiated than the neutral markers, suggesting local selection acting on them in a population-specific manner. On the basis of previous observations and the distribution of spotting phenotypes on a European scale, it is argued that thermal selection might operate on black spotting during the juvenile stages favouring more spots in continental climates. It is not clear what selective forces act on colour.     

Postembryonic development of the spider Enoplognatha ovata (Clerck) (Araneae:Theridiidae)

The postembryonic development of the three colour varieties of Enoplognatha ovata (CI.) was studied in the field and in the laboratory for two generations. Native and European spiders of this species were compared. Estimates of the number and duration of each stage were obtained from laboratory mating studies and verified by field studies. Males and females matured after five instars. Males matured faster than females but did not live as long. Each instar was characterized by several measurable parameters. All varieties over-winter in the second instar. Sexes could be easily separated at the fourth instar by comparing the ratio of the tarsal to patellar width of the pedipalps. Sexual dimorphism occurs at maturation ecdysis. Filial and mating studies indicate that the three colour varieties belong to a single species.     

The spider genus Enoplognatha (Araneae: Theridiidae) in Israel

Israeli theridiid spiders of the genus Enoplognatha are revised. Five species, four of them new, each represented by the two sexes, are recognized, and their affinities with similar species from adjacent regions are discussed. All species previously described from this region have been re-examined. The occurrence of E. mandibularis , formerly reported from Israel, has been confirmed, while the record of E. ovata has proved erroneous. A key to the species is provided.     

Stabilizing selection maintains exuberant colour polymorphism in the spider Theridion californicum (Araneae, Theridiidae)

Genetically controlled colour polymorphisms provide a physical manifestation of the operation of selection and how this can vary according to the spatial or temporal arrangement of phenotypes, or their frequency in a population. Here, we examine the role of selection in shaping the exuberant colour polymorphism exhibited by the spider Theridion californicum. This species is part of a system in which several distantly related spiders in the same lineage, but living in very different geographical areas, exhibit remarkably convergent polymorphisms. These polymorphisms are characterized by allelic inheritance and the presence of a single common cryptic morph and, in the case of T. californicum and its congener the Hawaiian happy-face spider Theridion grallator, numerous rare patterned morphs. We compare population differentiation estimated from colour phenotypic data to differentiation at neutral amplified fragment length polymorphisms (AFLP) loci and demonstrate that the colour polymorphism appears to be maintained by balancing selection. We also examine the patterns of selection in the genome-wide sample of AFLP loci and compare approaches to detecting signatures of selection in this context. Our results have important implications regarding balancing selection, suggesting that selective agents can act in a similar manner across disparate taxa in globally disjunct locales resulting in parallel evolution of exuberant polymorphism.     

Genetics and distribution of black spotting in Enoplognatha ovata (Araneae: Theridiidae), and the role of intermittent drift in population differentiation

Breeding studies have shown that the number of black spots on the dorsal surface of the opisthosoma of E. ovata is genetically determined, with a narrow heritability of about 0.7. There is, in addition, evidence that the presence and absence of spots might be under the control of a small number of major loci. Frequencies of spotted and non-spotted spiders in Nidderdale, Yorkshire, define the same three regions identified by previously studied variation at a regulatory locus. There are no correlations between sites in spotting and colour-morph frequencies. Variation in all three systems is independent of gross environmental factors. It is argued that the present-day patterns of genetic variation in these populations probably result from stochastic events during major environmental disturbance which is known to have occurred 40 years (generations) ago. Genetic drift, both continuous and intermittent, could be an important influence on morph frequencies in many E. ovata populations. Selection on conspicuous polymorphisms is not necessarily strong merely because the variation is conspicuous.     

Do current hypotheses explain continental and seasonal variation in female morph frequencies of the damselfly,Nehalennia irene?

Female-limited colour polymorphism occurs in many damselfly species, where one morph resembles the male (andromorph) and the other is dissimilar (gynomorph). Explanations for this phenomenon vary, but most assume that andromorphism has arisen in odonates, as a response to excessive male harassment. Here, we quantify the extent of continental and seasonal variation in female morph frequencies in a widely-distributed damselfly and ask whether the spatiotemporal patterns in andromorph frequency can be understood on the basis of sexual harassment theory. We sampled the damselfly, Nehalennia irene (Hagen) among regions across Canada, and at several sites, over the reproductive season, within Central Canada. Andromorph frequencies ranged from 0 to > 90% across Canada. In particular, sites in Western Canada had consistently high andromorph frequencies, whereas andromorph frequencies among Central sites were lower and variable and, among Eastern sites, were lower still (except one site) and relatively invariant. For populations in Central Canada, both andromorph frequencies and population densities varied significantly over time, reaching a peak mid-season. As expected, morph frequency covaried significantly with estimates of male harassment in some cases, but estimates of male harassment did not consistently account for variation in morph frequencies within all regions. Additional factors such as genetic drift may influence morph frequency at the edge of a species' range. Future work also should test, and attempt to explain causation, for seasonal variation in morph frequency.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 501–508.     

Natural selection in a postglacial range expansion: the case of the colour cline in the European barn owl

Gradients of variation—or clines—have always intrigued biologists. Classically, they have been interpreted as the outcomes of antagonistic interactions between selection and gene flow. Alternatively, clines may also establish neutrally with isolation by distance (IBD) or secondary contact between previously isolated populations. The relative importance of natural selection and these two neutral processes in the establishment of clinal variation can be tested by comparing genetic differentiation at neutral genetic markers and at the studied trait. A third neutral process, surfing of a newly arisen mutation during the colonization of a new habitat, is more difficult to test. Here, we designed a spatially explicit approximate Bayesian computation (ABC) simulation framework to evaluate whether the strong cline in the genetically based reddish coloration observed in the European barn owl (Tyto alba) arose as a by‐product of a range expansion or whether selection has to be invoked to explain this colour cline, for which we have previously ruled out the actions of IBD or secondary contact. Using ABC simulations and genetic data on 390 individuals from 20 locations genotyped at 22 microsatellites loci, we first determined how barn owls colonized Europe after the last glaciation. Using these results in new simulations on the evolution of the colour phenotype, and assuming various genetic architectures for the colour trait, we demonstrate that the observed colour cline cannot be due to the surfing of a neutral mutation. Taking advantage of spatially explicit ABC, which proved to be a powerful method to disentangle the respective roles of selection and drift in range expansions, we conclude that the formation of the colour cline observed in the barn owl must be due to natural selection.     

Microstructure of the silk apparatus of the comb-footed spider, Achaearanea tepidariorum (Araneae: Theridiidae)

The microstructural organization of the silk‐spinning apparatus of the comb‐footed spider, Achaearanea tepidariorum, was observed by using a field emission scanning electron microscope. The silk glands of the spider were classified into six groups: ampullate, tubuliform, flagelliform, aggregate, aciniform and pyriform glands. Among these, three types of silk glands, the ampullate, pyriform and aciniform glands, occur only in female spiders. One (adult) or two (subadult) pairs of major ampullate glands send secretory ductules to the anterior spinnerets, and another pair of minor ampullate glands supply the median spinnerets. Three pairs of tubuliform glands in female spiders send secretory ductules to the median (one pair) and posterior (two pairs) spinnerets. Furthermore, one pair of flagelliform glands and two pairs of aggregate glands together supply the posterior spinnerets, and form a characteristic spinning structure known as a “triad” spigot. In male spiders, this combined apparatus of the flagelliform and the aggregate spigots for capture thread production is not apparent, instead only a non‐functional remnant of this triad spigot is present. In addition, the aciniform glands send ductules to the median (two pairs) and the posterior spinnerets (12–16 pairs), and the pyriform glands feed silk into the anterior spinnerets (90–100 pairs in females and 45–50 pairs in males).     

State-dependent prey type preferences of a kleptoparasitic spider Argyrodes flavescens (Araneae: Theridiidae)

Spiders from the theridiid genus Argyrodes exhibit considerable variation in foraging tactics. However, little is known about the conditions under which Argyrodes spiders switch foraging tactics. Argyrodes flavescens (Pickard-Cambridge) is commonly found in the webs of another spider Nephila pilipes (Fabricius) in Singapore. In this study, a series of prey-choice tests were conducted for A. flavescens , both in the presence and absence of N. pilipes , to investigate the state-dependent prey type preference of A. flavescens . It was found that, in the absence of N. pilipes , well-fed A. flavescens took houseflies more than fruit flies, but starved A. flavescens took more fruit flies than houseflies. Whether N. pilipes spiders were present or absent, both well-fed and starved A. flavescens preferred living prey and rarely took wrapped prey of any kind. When well fed, A. flavescens rarely took mealworms. However, when starved, A. flavescens tended to take freshly captured prey, and also tended to feed together with N. pilipes on a housefly or mealworm captured by N. pilipes . Whether A. flavescens were absent or present, both well-fed and starved N. pilipes took mealworm larvae more often than they took houseflies, and they never attacked fruit flies. This is the first study to show that Argyrodes spiders alter their foraging tactics depending on hunger level, prey type, or the presence of the host. In doing so, Argyrodes spiders may maximize their energy gain and minimize predation risk in different circumstances.     

Trans-continental visible morph-frequency variation at homologous loci in two species of spider, Enoplognatha ovata s.s. & E. latimana

The spiders Enoplognatha ovata s.s. and E. latimana are sibling species which share a number of visible genetic polymorphisms. Data on colour and black-spotting morph frequencies in these species have been collected from 67 sites in western Europe. Sixty nine percent of the collections contained both species. In all adequately-sized samples, both species were polymorphic for colour and, in general, exhibited the same rank order of morphs lineata and redimita. (The top dominant morph, ovata, has not been found in E. latimana). Colour-morph frequencies are not correlated between species in sympatric populations from mainland Europe and from a previously studied area in Pembrokeshire, South Wales. Although associations with certain climatic variables are evident in E. ovata they are not consistent between transects, making their biological significance unclear. For black spotting, E. ovata s.s. is nearly fixed for spotting throughout mainland Europe but is highly variable in the Pembrokeshire populations. E. latimana is polymorphic in both areas. In Europe, spotting frequencies in E. latimana show significant associations with climatic factors but, again, their biological significance is not obvious. In E. ovata s.s. the variance in both colour and spotting frequencies among populations in Pembrokeshire is significantly greater than that in the whole of mainland Europe. The implications of these and previous results are considered in the context of the persistence of visible polymorphisms across species and the forces which determine morph frequencies in local populations.     

Population structure and dispersal in a patchy landscape: nuclear and mitochondrial markers reveal area effects in the spider Theridion californicum (Araneae: Theridiidae)

Changes in land use have a major effect on patterns of biodiversity. However, few studies have examined the demographic and genetic shifts associated with a return to semi‐natural habitat following extended periods of human disturbance. Here we examine patterns of population structure in a spider restricted to the Pacific coastal strip of North America that exhibits an exuberant colour polymorphism. We use mitochondrial DNA and AFLP markers to examine genetic structure and estimate gene flow. The results show contrasting, gender‐specific patterns between these markers that suggest limited dispersal, combined with area effects most likely caused by expansion from refugial habitat patches following land‐management changes in a region of the San Francisco East Bay. Colour‐morph frequencies are not correlated with this complex genetic structure. Thus, unlike the classical area effects that were based on colour morphs, we demonstrate in T. californicum signals of historical contingency at neutral loci but not at the Colour locus, where traces of past events have been obliterated by balancing selection. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 600–620.     

Genetic drift within a protected polymorphism: enigmatic variation in color-morph frequencies in the candy-stripe spider, Enoplognatha ovata

The candy-stripe spider, Enoplognatha ovata, exhibits a striking color polymorphism comprising three morphs. A number of lines of evidence strongly suggest that this polymorphism is maintained by natural selection: its presence in a sister species, E. latimana; the physical nature of the variation; the virtual lack of monomorphic populations; the highly consistent rank-order of morphs within populations; and the presence of large-scale clines associated with climatic variables. However, the absence of selection is equally strongly suggested by very local surveys of morph frequencies over space and time, perturbation experiments, and a variance in morph frequency between populations that is virtually independent of spatial scale. In addition, local spatial patterns in one study site (Nidderdale, Yorkshire, England) have been explained in terms of intermittent drift over half a century ago, a hypothesis supported here by the distributions of four other genetic markers (two allozyme and two visible polymorphisms). A heuristic model is suggested that reconciles these apparently contradictory messages regarding the importance of drift and selection in this system. It is proposed that when allele frequencies of the color morph redimita lie between approximately 0.05 and 0.3, the deltaq on q plot is very shallow, so that within this region, where the majority of populations lie, selection is weak and drift is the major force determining local morph frequencies. However, outside this range of frequencies, powerful selection acts to protect the polymorphism. This model may apply to polymorphisms in other species and explain why evidence of selection in natural populations is often elusive.     

Sexual selection and non-random mating for shell colour in a natural population of the marine snailLittorina mariae (Gastropoda: Prosobranchia)

In order to estimate the three independent components of mating behaviour, sexual selection in females, sexual selection in males and mating pattern, we studied the distribution of shell colour morphs among mating pairs and between copulating and non-copulating snails in four subsamples of a natural population ofL. mariae. The colour of the shell, the sex and a qualitative estimate of age was recorded for every snail. We found sexual selection acting against one of the two commonest colours (yellow) among the young females. However, in males none of the eight shell colour morphs was favoured during matings. Male sexual choice or differences in female sexual activity may cause the sexual fitness disadvantage of yellow females. Moreover, individuals of different colour morphs did not mate at random, rather dissasortatively. A behavioural choice among shell colour morphs or a non-random microdistribution of the morphs may cause the departure from random mating in this population.     

Host-dependent differences in prey acquisition between populations of a kleptoparasitic spider Argyrodes kumadai (Araneae: Theridiidae)

Abstract.  1. A kleptoparasitic spider, Argyrodes kumadai , is known to use phylogenetically unrelated host species in different regions – Cyrtophora moluccensis (Araneidae) in south-west Japan and Agelena silvatica (Agelenidae) in north-east Japan. The work reported here examined whether differences in host characters affect prey acquisition of A. kumadai .
2. Field surveys showed that prey-biomass capture rate of Argyrodes was significantly higher in populations parasitising Cyrtophora than in populations parasitising Agelena . Although Argyrodes appeared to catch fewer prey within Cyrtophora webs, they were able to feed upon substantially larger prey.
3. Differences in prey-biomass capture rate were found to reflect differences in host traits rather than regional differences in potential prey availability. Individuals in populations parasitising Cyrtophora were observed to acquire prey via a number of foraging tactics that included stealing wrapped food bundles, feeding upon prey remains and, in the case of large prey items, feeding together with the host. In contrast, individuals in populations parasitising Agelena were only ever observed to feed upon small prey items ignored by its host.
4. This variability in prey acquisition between kleptoparasite populations reflected different opportunities for feeding within their respective host webs – opportunities that were primarily determined by the foraging behaviour of the host. One key trait associated with host foraging behaviour was host-web structure, namely the presence/absence of a retreat.     

Effects of food deprivation on Latrodectus hasselti Thorell (Araneae: Theridiidae), the Australian redback spider

Abstract

Food deprivation tests indicate that most sub-adult and adult female Latrodectus hasselti spiders would be able to endure long periods of starvation if incarcerated in cargo. The data show that, under appropriate conditions, sub-adults survive for up to 160 days and some adults for more that 300 days. Temperature is an important variable with longevity being greatest at 10°C and markedly reduced at 25°C. Sluggishness is more pronounced at lower temperatures and probably reflects reduced metabolic rates. Even after 2–3 months without food, most spiders recover when fed.

Five stages mark the progress of starvation (Indices of Starvation) and reflect a gradual decline in the spider’s normal functions. As the abdomen shrinks, with a concomitant loss of hydraulic pressure, there is a gradual decline in web-building and locomotory activities which ultimately end in the spider’s death. It is assumed that nutritional deficiency and, to a lesser extent, dehydration contribute to mortality.     

The adaptive bases of ant-mimicry in a neotropical aphantochilid spider (Araneae: Aphantochilidae)

The aphantochilid spider Aphanlochilus rogersi accurately mimics black ants of tribe Cephalotini, and is commonly found in the neighbourhood of its models' nests. The mimic seems to be a specialized predator of this type of ant, rejecting any insect offered as prey other than cephalotines. In the field, A. rogersi was observed preying on the model species Zacryptocerus pusillus. In captivity, the spider preyed on the models Z. pusillus and Z. depressus, as well as on the yellow non-model Z. clypeatus. Recognition of correct prey by A. rogersi appears to be based primarily on visual and tactile stimuli. Capturing ant prey from behind was the most common attack tactic observed in A. rogersi, and is probably safer than frontal attacks, as in this case the spider can be bitten on the legs before the ant is immobilized. Aphanlochilus rogersi, when feeding on the hard-bodied ant models, uses the ant corpses as a ‘protective shield’ against patrolling ants of the victim's colony and resembles an ant carrying a dead companion. Certain types of mimetic traits in A. rogersi (close similarity to ant models in integument texture and pilosity of body and legs), together with ‘shielding behaviour’, are thought to function as ant-deceivers, facilitating the obligatory intimate contact the mimic must make with cephalotines in order to capture a prey among other ants. The close similarity in the arrangement of dorsal spines, body shape, integument brightness and locomotion, together with antennal illusion, is regarded as a strategy of A. rogersi for deceiving visually-hunting predators that avoid its sharp spined ant models. It is proposed that ant-mimicry in A. rogersi has both an aggressive and a Batesian adaptive component, and evolved as a result of combined selective pressures exerted both by Cephalotini ant models (through defensive behaviour towards the mimics which attack them) and predators that avoid cephalotines (through predatory behaviour toward imperfect mimics). This suggestion is schematized and discussed in terms of two tripartite mimicry systems.     

The role of selection in the colour polymorphism of Littorina rudis Maton and Littorina arcana Hannaford-Ellis (Prosobranchia: Littorinidae)

Forty-one mixed samples of winkles containing the closely related species, Littorina rudis and L. arcana , were collected from different parts of the British Isles. Littorina rudis was the more ubiquitous species, with L. arcana being more-or-less confined to vertical cliffs and rocks. The frequencies of different shell colour patterns were determined for both species in each sample. Several colour morphs were diagnostic of one or other of the species over large areas, which confirms that these are separate species. The frequencies, in the two species, of the two commonest morphs, brown and fawn, were strongly correlated; in several other morphs their presence and absence in the two species was significantly associated; the levels of phenotypic diversity in the two species were also correlated. These patterns could not have arisen if the variation between shores was the result of genetic drift or founder effects, so some form of selection is implicated. In the brown morph there is some evidence for frequency-dependent selection, and it is suggested that the polymorphism may be maintained by visual predators through apostatic selection.