Geoff S. Oxford

Genetics of colour and its regulation during development in the spider Enoplognatha ovata (Clerck) (Araneae: Theridiidae)

SummaryBreeding experiments have been performed to elucidate the genetics of colour and pattern in Enoplognatha ovata. The three main morphs, lineata, redimita and ovata, appear to be controlled by alleles at one locus. Red pigment in redimita and ovata may be deposited either in the third or fourth instars or at maturity. Patterns appearing early in development are found in both sexes whereas those appearing only at maturity are sex limited to females; males remain plain yellow (lineata). In mature females and some males, ovata is top dominant and lineata bottom recessive. Various genetic models of colour/pattern and its developmental control are explored.

Food induced esterase phenocopies in the snail Cepaea nemoralis.

SummaryHepatopancreatic extracts from the snail Cepaea nemoralis, assayed straight from the field, often contain three or four heavily staining esterase zones which migrate to the cathodal end of polyacrylamide disc gels during electrophoresis Previous breeding results showed that the heavily straining zones appeared allelic but to incorporate these multibanded phenotypes, a super gene of five closely linked loci was tentatively proposed. Further breeding work again failed to demonstrate multiple zones in parents or offspring and so experiments were conducted to see whether the multi-zoned phenotypes in the wild were produced by secondary modification of single primary products. Wild snails yielding extracts containing more than two heavily staining zones were shown to possess only two such zones after three months under laboratory conditions. Also, the ingestion of nettle (Urtica dioica L.) has been demonstrated to induce extra esterase zones in laboratory-reared animals. Some of the secondarily induced zones appear identical in physical, biochemical and electrophoretic properties to the primary products of other alleles, and thus appear to be electrophoretic phenocopies. A model is suggested which could account for this phenomenon.

Portraits of Evolution: Studies of Coloration in Hawaiian Spiders

Color variation, when genetically determined, provides a visual tool with which to investigate natural selection. Here we examine how color variation in two spider systems in the Hawaiian Islands can be used to understand evolutionary phenomena at both population and species levels. First, the happy-face spider (Theridion grallator) shows a number of discrete color morphs, the frequencies of which are very similar among populations, although the genetic basis for them differs between islands. These observations permit intriguing insights into the evolution and maintenance of color polymorphism. Second, we consider the adaptive radiation of Hawaiian Tetragnatha spiders. Here the spectacularly diverse array of color forms is found within closely related species on each island, with similar sets of colors evolving independently in each locale, suggesting selection is acting to maintain such diversity. Genetically determined color variation provides an immediately tangible link between a genotype and an externally expressed phenotype and, as a result, has long been used to probe evolutionary questions. In insects generally, and in Lepidoptera in particular, studies of color and pattern

De novo characterization of the gene-rich transcriptomes of two color-polymorphic spiders, Theridion grallator and T. californicum (Araneae: Theridiidae), with special reference to pigment genes

BackgroundA number of spider species within the family Theridiidae exhibit a dramatic abdominal (opisthosomal) color polymorphism. The polymorphism is inherited in a broadly Mendelian fashion and in some species consists of dozens of discrete morphs that are convergent across taxa and populations. Few genomic resources exist for spiders. Here, as a first necessary step towards identifying the genetic basis for this trait we present the near complete transcriptomes of two species: the Hawaiian happy-face spider Theridion grallator and Theridion californicum. We mined the gene complement for pigment-pathway genes and examined differential expression (DE) between morphs that are unpatterned (plain yellow) and patterned (yellow with superimposed patches of red, white or very dark brown).ResultsBy deep sequencing both RNA-seq and normalized cDNA libraries from pooled specimens of each species we were able to assemble a comprehensive gene set for both species that we estimate to be 98-99% complete. It is likely that these species express more than 20,000 protein-coding genes, perhaps 4.5% (ca. 870) of which might be unique to spiders. Mining for pigment-associated Drosophila melanogaster genes indicated the presence of all ommochrome pathway genes and most pteridine pathway genes and DE analyses further indicate a possible role for the pteridine pathway in theridiid color patterning.ConclusionsBased upon our estimates, T. grallator and T. californicum express a large inventory of protein-coding genes. Our comprehensive assembly illustrates the continuing value of sequencing normalized cDNA libraries in addition to RNA-seq in order to generate a reference transcriptome for non-model species. The identification of pteridine-related genes and their possible involvement in color patterning is a novel finding in spiders and one that suggests a biochemical link between guanine deposits and the pigments exhibited by these species.

The colour polymorphism in Enoplognatha ovatum (Clerck) (Araneae: Theridiidae)—Temporal stability and spatial variability

SummaryColonies of the visually polymorphic spider Enoplognatha ovatum have been studied in Nidderdale, Yorkshire, for up to six years. Morph frequencies are found to be stable within colonies between years but to vary between colonies only short distances apart. The stability of the polymorphism argues in favour of powerful selection acting on this character. The nature of the selective factors are unknown but they are not those which influence time of maturity of the spiders or the mature female population size, both of which have varied between years. A genetic basis proposed for the polymorphism is considered and rejected as being incompatible with stable morph frequencies.

The Evolution of Exuberant Visible Polymorphisms

Visible genetic polymorphism is a common feature of many species. In most cases, the mechanism(s) underlying the maintenance of such variation remain obscure although apostatic selection has often been suggested. Here, we explore individual-based evolutionary models to understand what features of predator-prey relationships may lead to patterns of exuberant polymorphism similar to those observed in the wild. When all morphs are equally visible, the number of evolved morphs increases with the strength of apostatic selection although even with powerful selection the number morphs is still relatively small. The introduction of dietary wariness increases the number of morphs substantially, even when apostatic selection is absent. When one morph is more cryptic the number of evolved morphs is fewer. The cryptic morph reaches high frequency in the population and other morphs are each at lower frequencies. Decreasing the predation intensity enhances the number of evolved morphs in all models. Dietary wariness is a critical factor missing from earlier models and it may provide a general solution to the problem of polymorphisms involving many morphs. Apostatic selection is shown to be neither a necessary, nor a sufficient, requirement for the maintenance of exuberant polymorphisms.

COLONIZATION HISTORY AND POPULATION GENETICS OF THE COLOR-POLYMORPHIC HAWAIIAN HAPPY-FACE SPIDER THERIDION GRALLATOR (ARANEAE, THERIDIIDAE)

Past geological and climatological processes shape extant biodiversity. In the Hawaiian Islands, these processes have provided the physical environment for a number of extensive adaptive radiations. Yet, single species that occur throughout the islands provide some of the best cases for understanding how species respond to the shifting dynamics of the islands in the context of colonization history and associated demographic and adaptive shifts. Here, we focus on the Hawaiian happy‐face spider, a single color‐polymorphic species, and use mitochondrial and nuclear allozyme markers to examine (1) how the mosaic formation of the landscape has dictated population structure, and (2) how cycles of expansion and contraction of the habitat matrix have been associated with demographic shifts, including a “quantum shift” in the genetic basis of the color polymorphism. The results show a marked structure among populations consistent with the age progression of the islands. The finding of low genetic diversity at the youngest site coupled with the very high diversity of haplotypes on the slightly older substrates that are highly dissected by recent volcanism suggests that the mosaic structure of the landscape may play an important role in allowing differentiation of the adaptive color polymorphism.

Geographical distribution of phenotypes regulating pigmentation in the spider Enoplognatha ovata (Clerck) (Araneae: Theridiidae)

The time when red pigment is deposited in the ovata and redimita morphs of Enoplognatha ovata is determined by a closely linked regulatory locus. In Nidderdale, Yorkshire, red pigment in the ovata morph is deposited early in development but the redimita pattern can develop either early or late. Phenotype frequencies at the regulatory locus define two main areas; one of which has a high and the other a very low frequency of the regulatory phenotype causing early production of red pigment. Phenotype frequencies at the regulatory locus and at the structural locus upon which it acts are not correlated. Bottlenecks in populations in the past might be responsible for allelic distributions at both loci, although selection cannot be excluded.

CONTRASTING PATTERNS OF HYBRIDIZATION IN LARGE HOUSE SPIDERS (TEGENARIA ATRICA GROUP, AGELENIDAE)

Abstract The integrity of species is not fixed and may vary geographically. Here we investigate the geographic distributions and interactions of species in the Tegenaria atrica group (Araneae: Agelenidae). Detailed mapping of T. saeva and T. gigantea in England and Wales shows them to be broadly allopatric in southern England with a tightly defined, and possibly long-standing, narrow zone of parapatry in central southern England. In the north of England (Yorkshire), by contrast, the species are broadly sympatric as a result of recent range expansions. GIS techniques are used to map the species distributions and to quantify, we believe for the first time, the intimacy of interspecific interactions. The extent and nature of hybridization in these two areas is examined through regression and multivariate analyses of morphology. We show that the relative incidence of hybridization is much greater in Yorkshire than within the parapatric zone in the south. Clear patterns of asymmetric introgression are observed in both northern and southern England, with a greater impact of T. gigantea on T. saeva than vice versa. We find no sign of morphological reproductive character displacement at the zone of parapatry that might indicate reinforcement, although we cannot exclude more subtle effects, for example via cuticular pheromones. The integrity of these two species seems to be breaking down in northern England, a process that might gain momentum as the gene pools become more similar.

Visible morph-frequency variation in allopatric and sympatric populations of two species of Enoplognatha (Araneae : Theridiidae)

Samples were taken from single- and mixed-species populations of two spiders, Enoplognatha ovata and E. latimana, which share visible polymorphisms. The range of colour-morph frequencies was comparable between the species but E. latimana had a uniformly lower proportion of individuals with black spots. Spotted E. ovata females were more likely to have cocoons when collected than females without spots, although in spotted individuals there was no relationship between presence of cocoons and spot number. Colour-morph frequencies varied both within and between the seven study areas, sometimes over very short distances. A similar, though less marked, pattern was shown by the black spotting phenotype. This variation, on two geographical scales, was present in both species. No evidence was found for consistent shifts in morph frequencies between allopatric and sympatric populations, and morph frequencies were not correlated between species across sympatric populations. Thus, common selective agents acting on the polymorphisms could not be demonstrated, although species-specific factors cannot be eliminated. It is possible that stochastic processes influence local morph frequencies, as has been suggested for E. ovata elsewhere.