The distribution of bumblebee colour patterns worldwide: possible significance for thermoregulation, crypsis, and warning mimicry

Bumblebee colour patterns can be highly variable within species, but are often closely similar among species. The present study takes a quantitative approach to survey bumblebee colour patterns in order to address some of the most basic questions concerning resemblances: (1) do colour‐pattern groups exist; (2) are species within colour‐pattern groups geographically clumped; and (3) are some colour‐pattern groups associated with particular kinds of habitat? The results using data for 632 worker patterns from all of the world’s bumblebee species show that: (1) there are many repeating colour patterns, forming relatively few groups of species with similar patterns; (2) colour‐pattern groups can be recognized using simple rules; and (3) species within the 24 largest colour‐pattern groups are significantly aggregated in particular areas of the world. Three principal divisions of colour‐pattern groups are associated with three likely functions: (1) the darkest bumblebees are associated primarily with the tropics, where a thermoregulatory function is suggested; (2) the palest bumblebees are associated with intermediate northern latitudes, where a cryptic function in drying grasslands is suggested; and (3) the intermediate, strongly banded bumblebees are widespread, although these patterns predominate where banding may have advantages as collective warning signals to predators (Müllerian mimicry). Further studies are needed to test these explanations. © The Natural History Museum, London. Journal compilation © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92 , 97–118.     

The Role of Early Learning in Determining Shoaling Preferences Based on Visual Cues in the Zebrafish, Danio rerio

Social preferences for specific colour patterns learned in early development, termed imprinting, may influence social and mating decisions. Imprinting has been demonstrated in both birds and fish and has been proposed to play a role in speciation. We raised wild‐type zebrafish, Danio rerio, either with individuals of the same colour pattern, an alternative colour pattern (leopard), or a closely related, unpatterned species, D. albolineatus. We also cross‐reared individual ‘leopard’D. rerio and D. albolineatus with wild‐type D. rerio. We tested the prediction that Danio would prefer to shoal with fish of the colour pattern with which they had been raised, irrespective of their own appearance. Rearing condition affected shoaling preferences between D. rerio and D. albolineatus, with individuals of both colour patterns preferring to associate with shoals of the colour pattern with which they had been raised. The more subtle distinction between the wild‐type and ‘leopard’D. rerio colour patterns did not elicit a shoaling preference. Thus, zebrafish exhibit shoaling preferences based on visual cues, the effect being stronger when patterns are more distinct. There is a strong learned component to these preferences, although the extent to which they may influence mating decisions is unclear.     

Defining the colour pattern phenotype in bumble bees (Bombus): a new model for evo devo

Few insects exhibit the striking colour pattern radiation found in bumble bees (Bombus), which have diversified globally into a wide range of colours and patterns. Their potent sting is often advertised by conspicuous bands of contrasting colour commonly mimicked by scores of harmless (Batesian mimics) and noxious species (Müllerian co‐mimics). Despite extensive documentation of colour pattern diversification, next to nothing is known about the genetic regulation of pattern formation in bumble bees, hindering progress toward a more general model of the evolution of colour pattern mimicry. A critical first step in understanding the colour pattern genotype is an unambiguous understanding of the phenotype under selection, which has not been objectively defined in bumble bees. Here, we quantitatively define the principal colour pattern elements that comprise the phenotype array across all species. Matrix analysis of meticulously scored colour patterns of ～95% of described species indicates there are 12 discrete primary ‘ground plan’ elements in common among all species, many of which correspond to segmentation patterning. Additional secondary elements characterize individual species and geographical variants. The boundaries of these elements appear to correspond to expression patterns of Hox genes in Drosophila and Apis but also suggest novel post‐Hox specialization of abdominal patterning. Our findings provide the first foundation for exploring candidate genes regulating adaptive pattern variation in bumble bees and broaden the framework for understanding common genetic mechanisms of pattern evolution in insects. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 384–404.     

Variation and seasonal changes in hoverfly species: interactions between temperature, age and genotype

Eristalis tenax L. and E. intricarius L. are two hoverflies which vary considerably in colour pattern. Whilst much of the phenotypic variation in both species is due to genetic variation at major gene loci, there are interactions with pupal temperature and with age of adult. Low pupal temperatures produce, on average, darker abdominal patterns in E. tenax , although the effect is hard to pick out in natural populations. Changes of pattern with age convert a bimodal autumn population to a unimodal post-hibernation population in the following spring. Hair colour is also made darker by cold treatment. Pupal treatments have a strong effect on hair colouration in E. intricarius. High temperatures inhibit the production of black hairs on the thorax, but not all the genotypes are equally sensitive to temperature. Seasonal fluctuations in colour pattern frequencies are detectable in E. intricarius. In three Eristalis species that have been studied so far, the interactions between genotype, age and temperature operate in quite different ways. The temperature responses may be relevant to theories of thermal melanism, although the colour pattern polymorphisms are, more obviously, examples of Batesian mimicry.     

Phylogeography of colour polymorphism in the coral reef fish Pseudochromis fuscus, from Papua New Guinea and the Great Barrier Reef

Body colour has played a significant role in the evolution of coral reef fishes, but the phylogenetic level at which colour variation is expressed and the evolutionary processes driving the development and persistence of different colour patterns are often poorly understood. The aim of this study was to examine the genetic relationships between multiple colour morphs of Pseudochromis fuscus (family Pseudochromidae), both within and among geographic locations. Pseudochromis fuscus is currently described as a single species, but exhibits at least six discrete colour morphs throughout its range. In this study, P. fuscus from Papua New Guinea (PNG) and the Great Barrier Reef (GBR), Australia, formed three genetically distinct clades based on mitochondrial DNA (control region) sequence data: (1) yellow and brown morphs from the GBR and southern PNG, as well as an orange morph from southern PNG; (2) a pink morph from southern PNG; and (3) all three morphs (pink, orange and grey) found in Kimbe Bay, northern PNG. The three groups showed deep levels of divergence (d=14.6–25.4%), suggesting that P. fuscus is a complex of polychromatic species, rather than a single widespread species with many different colour morphs. Population genetic analyses indicate that the three clades have experienced unique evolutionary histories, possibly from differential effects of sea level fluctuations, barriers to gene flow and historical biogeography.     

Coral snake mimicry: live snakes not avoided by a mammalian predator

The occurrence of coral snake coloration among unrelated venomous and non-venomous New World snake species has often been explained in terms of warning coloration and mimicry. The idea that snake predators would avoid coral snakes in nature seems widely established and is postulated in many discussions on coral snake mimicry. However, the few workers that have tested a potential aposematic function of the conspicuous colour pattern focused exclusively on behaviour of snake predators towards coloured abstract models. Here we report on behaviour of temporarily caged, wild coatis (Nasua narica) when confronted with co-occurring live snakes, among which were two species of venomous coral snakes. Five different types of responses have been observed, ranging from avoidance to predation, yet none of the coatis avoided either of the two coral snake species or other species resembling these. As in earlier studies coatis appeared to avoid coral snake models, our findings show that results from studies with abstract snake models cannot unconditionally serve as evidence for an aposematic function of coral snake coloration.     

A generalised mimicry system involving angiosperm flower colour, pollen and bumblebees’ innate colour preferences

Flower colour is a major advertisement signal of zoophilous plants for pollinators. Bees, the main pollinators, exhibit innate colour preferences, which have often been attributed to only one single floral colour, though most flowers display a pattern of two or several colours. The existing studies of floral colour patterns are mostly qualitative studies. Using a model of bee colour vision we quantitatively investigate two questions: whether or not component colours of floral colour patterns may mimic pollen signals, and whether or not bumblebees exhibit innate preferences for distinct parameters of naturally existing floral colour patterns. We analysed the spectral reflectances of 162 plant species with multicoloured flowers and inflorescences, distiniguishing between inner and outer colours of floral colour patterns irrespective of the particular structures so coloured.We found that:– The inner colour of radially symmetrical flowers and inflorescences and of zygomorphic flowers appears less diverse to bees than the peripheral colour.– The inner colour of most radial flowers and inflorescences as well as the inner colour of a large number of non-related zygomorphic flowers appears to bees to be very similar to that of pollen.– Bumblebees (Bombus terrestris) exhibit innate preferences for two-coloured over single-coloured dummy flowers in a spontaneous choice test.– Bumblebees exhibit innate preferences for dummy flowers with a large over those with a small centre area.– Bumblebees exhibit innate preferences for dummy flowers with a centre colour similar to that of pollen over those with another centre colour.Our findings support the hypotheses that the inner component of floral colour patterns could be interpreted as a generalised and little recognised form of mimicry of the colour of visually displayed pollen, that bumblebees exhibit innate preferences regarding colour and size parameters of floral colour patterns, and that these correspond to visually displayed pollen. These findings together suggest a prominent role of floral colour patterns in advertisement to and guidance of naive flower visitors.     

The effects of various fixatives on subsequent lectin binding to tissue sections

Summary The effects of ten fixation protocols on the subsequent binding of eight lectins to various mouse tissue sites have been systematically evaluated. The fixatives used were neutral and buffered formalin—saline, Bouin's fluid, 95% ethanol, Carnoy's fluid, calcium acetate—paraformaldehyde, and mercuric chloride both before and after removal of mercury pigment. These were compared with frozen sections of unfixed tissue and frozen sections post fixed in paraformaldehyde. Lectins used were PNA, DBA, SBA, BPA, UEA 1, GS I, GS II and MPA. Ethanol was found to be the superior fixative, closely followed by mercuric chloride. Paraformaldehyde was a poor fixative of both paraffin and frozen sections. It is recommended that, where a choice is possible, the fixation protocol appropriate to the particular lectin and tissue binding site is selected. Within certain limitations, formalin—saline proved an adequate fixative for the study of routine paraffin-processed tissue sections.     

Eggshell coloration is an indicator of dietary calcium in Common Pheasants (Phasianus colchicus)

According to the structural-function hypothesis, the eggshell pigment protoporphyrin, deposited at weak spots, can strengthen the shell structure when calcium is lacking in avian species. However, this hypothesis has not been tested in species that produce pigmented eggs of uniform ground colour without spotting patterns. We tested the structural-function hypothesis using 435 eggs produced on seven calcium diets (0.2–4.5%) given to Common Pheasants Phasianus colchicus, a species that produces a large number of eggs on a low-calcium diet with unspotted eggshells composed of a uniform ground colour of mainly protoporphyrin. We found that pheasants on the lowest calcium diet (0.2%), which had thinner eggshells, produced eggs containing more protoporphyrin-based coloration than four of six other diets, suggesting this species employs pigmentation as ground colour to strengthen eggshells when available calcium is low. Our results provide the first, at least partial support for a structural function for eggshell pigments producing ground colour without spotting in a species that is often calcium-limited. This pattern may be more widespread in other ground-nesting taxa that also produce large numbers of eggs with protoporphyrin-based ground colour and are potentially limited by calcium during breeding.     

The genetic basis of an adaptive radiation: warning colour in two Heliconius species

Mimetic colour pattern races of Heliconius butterflies provide a striking example of adaptive radiation and numerous crossing experiments have investigated the genetics of these racial differences. However, colour pattern differentiation between closely related Heliconius species has not been previously studied. Here we present data from crosses between H. erato cyrbia and its sister species, H. himera. The genetic architecture underlying colour pattern divergence between these species is identical to that observed between races of H. erato. As in inter-racial crosses, colour pattern differences resulted from segregation at a few major loci. Evidence from 1321 offspring in 4 F₁, 17 backcross, 7 F₂ and 21 further crosses showed that two major loci controlled most of the colour pattern differences between H. erato and H. himera. There were strong interactions between these loci in their patterns of expression and evidence for other loci with relatively minor phenotypic effects. More importantly, based on patterns of expression within broods and linkage with Aconitase, we conclude that these major loci were homologous with those known to be responsible for colour pattern differences within H. erato. Our crosses also permit a re-evaluation of the relationships between colour pattern races of H. erato. This suggests that H. e. hydara, which occurs across a major mtDNA break, is the ancestral phenotype from which other races have evolved. Based on this assumption, we find no evidence to support the recent suggestion that apparently homologous colour pattern alleles have arisen multiple times.     

Rare piebald and partially leucistic Antarctic fur seals, <Emphasis Type="Italic">Arctocephalus gazella</Emphasis>, at Cape Shirreff,Livingston Island,Antarctica

We document five cases of unusual colouration in Antarctic fur seals, Arctocephalus gazella, at Cape Shirreff, Livingston Island, from 1991–1992 to 2005–2006 austral summer seasons. This is the first time that these colour patterns have been reported for this species. These included four rare light coloured animals and one piebald individual. The incidence of this atypical colouring was low and the lack of resightings in previous and subsequent seasons suggests that these morphs are not common in Antarctic fur seals. Although the causes of these atypical light colour patterns are uncertain the subject is interesting for study and more observations on these atypical colourations are required for a proper assessment of the ecological and physiological implications of this condition in otariids can be conducted in the future.     

A new species of Nidalia Gray, 1835 from Mid-Atlantic seamounts (Octocorallia, Alcyonacea, Nidaliidae)

A new soft coral species of the genus Nidalia, from seamounts to the south of the Azores Archipelago is described. The main features of Nidalia aurantia n. sp. are as following: colony torch-like, a capitulum light orange in colour, not laterally flattened, dome-shaped and not distinctly projecting beyond the stalk, an introvert with sparse sclerites transversally placed, and an anthocodial crown with 13–17 sclerite rows. The new species is compared with its closest congeners. This is the first time that a species of Nidalia has been located in the Mid-Atlantic Ocean.     

Effects of freezing on white perch Morone americana (Gmelin, 1789): implications for multivariate morphometrics

This study tested the hypothesis that duration of freezing differentially affects whole‐body morphometrics of a derived teleost. Whole‐body morphometrics are frequently analyzed to test hypotheses of different species, or stocks within a species, of fishes. Specimens used for morphometric analyses are typically fixed or preserved prior to analysis, yet little research has been done on how fixation or preservation methods or duration of preservation of specimens might affect outcomes of multivariate statistical analyses of differences in shape. To determine whether whole‐body morphometrics changed as a result of freezing, 23 whole‐body morphometrics of age‐1 white perch (Morone americana) from western Lake Erie (n = 211) were analyzed immediately after capture, after being held on ice overnight, and after freezing for 100 or 200 days. Discriminant function analysis revealed that all four groups differed significantly from one another (P < 0.0001). The first canonical axis reflected long‐axis morphometrics, where there was a clear pattern of positive translation along this axis with duration of preservation. Re‐classification analysis demonstrated fish were typically assigned to their original preservation class except for fish frozen 100 days, which assigned mostly to frozen 200 days. Morphometric comparisons using frozen fish must be done on fish frozen for identical periods of time to avoid biases related to the length of time they were frozen. Similar experiments should be conducted on other species and also using formalin‐ and alcohol‐preserved specimens.     

The tail tells the tale: taxonomy and biogeography of some Atlantic Chelidonura (Gastropoda: Cephalaspidea: Aglajidae) inferred from nuclear and mitochondrial gene data

Several western Atlantic species of Chelidonura have been described mainly based on differences in colour pattern. Sequence data from two mitochondrial [cytochrome oxidase I (COI), 16S] genes and a nuclear [histone 3 (H3)] gene have revealed that all colour forms previously recognized from across the Caribbean, Bahamas, and Bermuda belong to the same species, Chelidonura berolina. However, several specimens from the Bahamas are genetically and morphologically distinct and are herein described as a new species, Chelidonura normani sp. nov. Externally, C. normani can only be distinguished from C. berolina by the morphology of the posterior end of the body and not by colour pattern. Both C. berolina and C. normani are genetically and morphologically distinct from the eastern Atlantic species Chelidonura africana, but the split between C. berolina and C. normani predates the split between C. berolina and C. africana. All three species differ in their protoconch morphology, which suggests different developmental modes. Furthermore, all three species display a broad variation in colour pattern, which raises questions on the biological significance of colour in this group. The reasons for the divergence between C. berolina and C. normani remain unknown but could be related to the complex geological history of the western Atlantic. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163 , 1077–1095.     

Variable colour patterns indicate multidimensional,intraspecific trait variation and ecological generalization in moths

Animal colour patterns long have provided information about key processes that drive the ecological and evolutionary dynamics of biological diversity. Theory and empirical evidence indicate that variation in colour patterns and other traits among individuals generally improves the performance of populations and species, for example by reducing predation risk, increasing establishment success, improving resilience to environmental change, and decreasing risk of extinction. However, little is known about whether and how variation in colour pattern among species is associated with variation in other phenotypic dimensions. To address this issue, we analysed associations of colour pattern with morphological, behavioural and life-history traits on the basis of data for nearly 400 species of noctuid moths. We found that moths with more variable colour patterns had longer flight activity periods, more diverse habitats and a greater number of host plant species than species with less variable colour patterns. Variable coloration in adult noctuid moths therefore can be considered as indicative of broader niches and generalist diets. Colour pattern variability was not significantly associated with overwintering stage or body size (wing span), and it was independent of whether the colour pattern of the larvae was non-variable, variable or highly variable. Colour pattern variation during the larval stage tended to increase as the duration of the flight activity period increased, but was independent of the length of the larval period, diet breadth and habitat use. The realization that information on colour pattern variation in adult moths, and possibly other organisms, offers a proxy for niche breadth and dietary generalization can inform management and conservation biology.     

Seed colour and post-fire bird predation in a Mediterranean pine forest

In a Pinus halepensis Mill. forest, a field experiment was designed to evaluate post-fire seed predation as affected by combinations of seed colour and soil substrates: light grey and black seeds combined with light grey ash, dark grey ash and pale brown sand. A survey of bird species inhabiting the area was also carried out and polyphenolic content of seed coat was assessed in seed lots of different colour. Light grey seeds were observed to be less predated on light grey ash, suggesting eucrypsis as a protective strategy against bird predation. On the contrary, no clear pattern was observed for the predation of black seeds on different substrates. In the study area both bird species breaking the seed coat and eating the endosperm and bird species swallowing the whole seed were monitored. We have estimated that more seeds were swallowed than broken, in all colour categories. Light grey seeds, which were found to have a higher content of polyphenols, were predated more than black seeds when exposed on the same substrate. Thus, no evidence was produced that the amount of polyphenols in seed coat could protect seeds from predation.     

Phylogenetic and biogeographic analysis of the spear lobsters Linuparus (Decapoda: Palinuridae), with the description of a new species

Linuparus White, 1847 comprises three extant species, Linuparus trigonus (Von Siebold, 1824), L. sordidusBruce, 1965, and L. somniosusBerry and George, 1972, as well as 32 fossil species. Most fossil records are from North America and Europe, but the extant species are all confined to the Indo-West Pacific. Different colour forms in L. trigonus and L. sordidus have been noted, with Northern Hemisphere specimens generally darker in colour for both species. The phylogenetic relationships of the extant Linuparus species, including the colour forms, were investigated using mitochondrial 12S rRNA and COI gene sequence analysis. We found no genetic evidence to differentiate the colour morphs of L. sordidus, but the two colour forms of L. trigonus were clearly distinct at the species level. This is supported morphologically by a consistent difference in the shape of the thoracic sternum between the two forms. The paler coloured Southern Hemisphere form is described as a new species, L. meridionalis. Phylogenetic analysis shows that L. trigonus and L. meridionalis sp. nov. are derived sister taxa, while L. somniosus is basal within the genus. Thus the present results support the previous hypothesis that Linuparus was originated in shallow water.     

Female mate choice and species recognition between two closely related cichlid fish of Lake Malawi,Metriaclima estherae and M. callainos

Cichlids are one of the most diverse and colourful groups of freshwater fishes in the world. Despite much investigation, the factors that promote speciation in these fishes are still uncertain. However, previous studies suggest that sexual selection on male colour is one of the main drivers of speciation among these fishes. Metriaclima estherae is a polymorphic cichlid species from Lake Malawi, and thus provides an ideal model for the investigation of the importance of colour as a species recognition cue. M. callainos is a closely related and morphologically similar species, with male colour pattern very similar to that of M. estherae. We tested female choice by giving females of the two species a choice between conspecific and heterospecific males in the presence and absence of visual (colour) and chemical cues. The results show that females of M. callainos were able to reliably recognize conspecific males, even when colour was eliminated as a cue. However, females of M. estherae did not prefer conspecific males, although they were able to discriminate between red and blue conspecific colour morphs by using chemical cues. These results suggest that species recognition cues may differ even among closely related species of cichlid fish, and that female preferences for male coloration may be weak in certain species.