Change and stability in a steep morph‐frequency cline in the snail Cepaea nemoralis (L.) over 43 years

Populations of the polymorphic land snail Cepaea nemoralis (L.) from Deepdale, Derbyshire, UK, sampled in 1965–67, showed a pattern of area effects, with steep clines among groups of populations differing in shell colour and banding morph frequencies. In 2010, most of these populations were resampled. In particular, a continuous transect made in 1967 of 42 quadrats (18.34 × 18.34 m) across a steep cline in several morph frequencies was completely resampled. In the dale as a whole, yellow shells had increased in frequency. In the transect, the frequencies of banding morphs showed no significant changes, although colour morphs showed some changes. Pink shells had increased in frequency in a section in which scrub had developed, and brown shells had increased in frequency in the area in which they had originally been at the highest frequency. In each case, the selection coefficients were of the order of 4%. Yellow had increased elsewhere. Nevertheless, both in the dale as a whole and in the transect, the pattern of geographical change in morph frequencies had remained essentially the same. Estimates of migration based on previous studies of marked snails and on modelling of the effect of drift and migration suggest that, regardless of whether the cline is a product of differential selection or of the gradual merging of previously separate founding populations, it has been in existence for a long time, and that migration occurs over greater distances than estimated from direct observation on marked snails. Although we can demonstrate that selection has occurred, the origin and maintenance of the cline and others similar to it remain in doubt; the development and maintenance of polymorphism in this species may require consideration of several processes operating on different time scales. © 2012 The Linnean Society of London     

Camouflaged invasion of Lake Malawi by an Oriental gastropod

In this study we report the first animal invasion, to our knowledge, into Lake Malawi. The colonizer is a non-native morph of the gastropod Melanoides tuberculata that differs substantially in external shell characters from co-occurring indigenous forms. However, because the species possesses extensive within-Africa geographical variation in shell morphology, it was unclear whether the invasion was range expansion of a native African morph, or a colonization from elsewhere. Mitochondrial DNA sequences indicate a southeast Asian origin for the invader, suggesting that shell variation found among indigenous allopatric populations camouflaged an intercontinental invasion.     

The evolution of extreme shell shape variation in the land snail Ainohelix editha: a phylogeny and hybrid zone analysis

Ainohelix editha from Hokkaido, Japan, exhibit great geographical variation in their shell morphology. In particular, A. editha in two quite separate locations, Shimamaki and Samani, are striking because they are extremely flat and have a sharp keel, whereas at adjacent sites the shells are globular or depressed-globular. We used mitochondrial 16S rRNA and nuclear ITS-2 sequences to infer a phylogeny among 47 snails from 29 locations. Snails from the two keeled-flat populations clustered separately in the phylogeny, suggesting that this unusual shell form could have evolved independently. A morphological analysis of shells collected along a transect between keeled-flat and globular snail sites showed a cline for shell shape and the angle of the keel. Two different mtDNA lineages were found across the transect, with a cline for an ITS-2 single nucleotide polymorphism. Together, the results may suggest a lack of reproductive isolation between keeled-flat and globular snails, with possible introgression by hybridization.     

The wave speed of intergradation zone in two-species lattice Müllerian mimicry model

A spatially explicit model is studied to analyse the movement of coupled clines in two-species Müllerian mimicry system as exemplified by the comimicking helicoiine butterflies in Central-South America Heliconius erato and Heliconius melpomene. In this system, a pair of comimicking wing patterns of two species (mimicry ring) is found in a geographical region but another pair of wing patterns is found in a different geographical region. The distribution of mimicry rings thus forms a spatial mosaic in a large geographical scale, and the mechanism responsible for their stable maintenance has been a long-standing question in evolutionary biology. We here examine the speed of the movement of boundaries that divide the regions inhabited by different mimetic morphs in each comimicking species, by assuming coupled two-state stochastic cellular automatons where the flipping rate of the site occupied by a mimetic morph depends on the local density of the same morph and of the comimicking morph in the other species. The speed of cline movement shows a complex dependence on the coupling parameter between mimetic species--greater coupling of comimicking morphs between species slows down the cline movement only when the reduction in predation rate exhibits diminishing return to the increase of local mimetic morph density. The analytical predictions are confirmed by the results of Monte Carlo simulations. The speed of advance is quite different from that predicted from the conventional reaction-diffusion model, indicating that demographic stochasticity plays a critical role in determining the speed of cline movement. We also examine if the spatial heterogeneity in migration rate can stably maintain clines.     

Colour polymorphism in the intertidal snail Littorina rudis Maton

The tictors affecting the variation of shell colour morph frequencies of the intertidal snail Littorina rudis Maton have been examined using ordination and correlation techniques. The major gradient underlying variation in shell colour is related to habitat type and structure. Dark, patterned shells are characteristic of cliff and salt marsh habitats whilst light, unpatterned shells reach high frequencies on boulder shores. Colour morphs do not differ significantly in shell thickness and between-shore variation in colour morph frequencies cannot be directly attributed to habitat dilterences in the risk of shell injury, but to other factors associated with habitat type and structure, e.g. parasitism. It is suggested that the maintenance of shell colour polymorphism in L. rudis is probably mediated by selection on pleiotropic characters rather than shell colour alone.     

Contribution of molecular phylogeny and morphometrics to the systematics of African elephants

African elephants are conventionally classified as a single species: Loxodonta africana (Blumenbach 1797). However, the discovery in 1900 of a smaller form of the African elephant, spread throughout the equatorial belt of this land, has given rise to a debate over the relevance of a second species of elephant in Africa. The twentieth century has not provided any definite answer to this question. Actually, recent molecular analyses have sustained this issue by advocating either a division of forest elephants into a valid species, or their inclusion as a subspecies of L. africana. Our work initiated at the National Museum of Natural History of Paris provides new molecular (mitochondrial) and morphological (and morphometrical) evidence making it possible to propose a comprehensive phylogenetic hypothesis. It appears that there is no conclusive argument to keep forest elephants (cyclotis form) and savannah elephants (africana form) apart in two distinct species. A high level of mitochondrial introgression between the two forms, as well as a continuum in the morphology of the skulls of the two morphotypes rather suggests that, despite an ancient division, these two taxa freely interbreed wherever their ranges intersect. We thus adopt a conservative systematic position in considering these two forms as two subspecies, respectively: L. africana africana, the savannah elephant, and L. africana cyclotis, the forest elephant. We finally discuss the conservation topic in the light of this systematic framework.     

Clinal variation in the morph ratio of Black Sparrowhawks Accipiter melanoleucus in South Africa and its correlation with environmental variables

The morph ratio distribution in polymorphic species often varies clinally, with a gradual change in morph ratios across the distributional range of the species. In polymorphic bird populations, clinal variation is rarely quantified. We describe a cline in the morph ratios of Black Sparrowhawks across South Africa, which is principally driven by a higher ratio of dark morph birds in the newly colonized southwest of the country. Across the 1400 km of our cline, the probability of a bird being a dark morph declined from over 80% close to the Cape Peninsula to under 20% in the northeast. Higher frequencies of dark morphs were associated with a higher proportion of rainfall falling during the winter breeding months. Further investigation revealed relationships between the proportion of dark morphs and altitude, amount of rainfall during the breeding months, and an interaction between this variable and temperature. These results provide some support for the suggestion that the higher frequency of dark morphs in the southwest is an adaptive response, rather than the result of a founder effect or genetic drift. These findings also suggest that, in theory, polymorphic species may be better adapted to cope with the challenges of climate change or may be able to expand their ranges more quickly into novel climatic areas, since selection pressure can act on a pre‐existing trait that may be beneficial in new conditions.     

PREDATOR-INDUCED SHELL DIMORPHISM IN THE ACORN BARNACLE CHTHAMALUS ANISOPOMA

Field experiments were conducted in order to determine the nature of shell dimorphism in the acorn barnacle Chthamalus anisopoma and the adaptive significance of the atypical form. The typical morph has the conical shape which is characteristic of acorn barnacles, while the atypical morph appears bent over, with the rim of its aperture oriented perpendicular to its base. The experiments showed that: 1) the bent-over morphology is an environmentally-induced developmental response to the presence of a carnivorous gastropod (Acanthina angelica) and 2) that “bents” are more resistant than “conics” to specialized predation by this snail. The results also showed that predation by A. angelica is patchy and heaviest in the near vicinity of cracks and crevices, which it uses as refuges during periods of tidal inundation. Because predation is patchy and bents are less fecund and grow slower than conics, the conditional developmental strategy is likely to be favored over strict genetical control of shell morphology.     

Correlated evolution of floral morphology and mating-type frequencies in a sexually polymorphic plant

In sexually polymorphic species, reproductive morphology governs mating patterns and the character of negative frequency-dependent selection. If local environmental conditions cause sexual morphs to differ between populations, then frequency-dependent selection should create corresponding geographic variation in morph frequencies. We investigate this relation with a model of morph-ratio evolution and analysis of geographic variation in the heterostylous plant Narcissus triandrus. Unlike other tristylous species, N. triandrus possesses both imperfect reciprocity among morphs in sex-organ position and a self-incompatibility system that permits outcrossing within and between morphs. We sampled 137 populations throughout the Iberian Peninsula for floral-morph ratios, and measured floral morphology in 31 populations. Morph ratios exhibited three atypical features: (1) predominance of the long-styled (L) morph; (2) absence of the mid-styled (M) morph from 17.5% of populations; and (3) a negative relation between the frequencies of the L and M morphs among populations. Morph ratios varied geographically, with decreasing frequency of the M morph from the southeast to the northwest of the species' range. Much of this variation accompanied allometric change in the positions of sex organs, especially the mid-level organs, with the M morph declining in frequency and ultimately being lost in large-flowered populations. Using multivariate multiple regression, we demonstrate that variation in floral morphology among populations predicts this geographic variation in morph frequencies. Our theoretical analysis illustrates that patterns of pollen transfer governed by imperfect sex-organ reciprocity can select for unequal equilibrium morph ratios like those observed for N. triandrus. We interpret the L-biased morph ratios and the unusual morphology of N. triandrus as a consequence of its atypical intramorph compatibility system.     

Adaptation to a steep environmental gradient and an associated barrier to gene exchange in Littorina saxatilis

Steep environmental gradients offer important opportunities to study the interaction between natural selection and gene flow. Allele frequency clines are expected to form at loci under selection, but unlinked neutral alleles may pass easily across these clines unless a generalized barrier evolves. Here we consider the distribution of forms of the intertidal gastropod Littorina saxatilis, analyzing shell shape and amplified fragment length polymorphism (AFLP) loci on two rocky shores in Britain. On the basis of previous work, the AFLP loci were divided into differentiated and undifferentiated groups. On both shores, we have shown a sharp cline in allele frequencies between the two morphs for differentiated AFLP loci. This is coincident with a habitat transition on the shore where the two habitats (cliff and boulder field) are immediately contiguous. The allele frequency clines coincide with a cline in shell morphology. In the middle of the cline, linkage disequilibrium for the differentiated loci rises in accordance with expectation. The clines are extremely narrow relative to dispersal, probably as a result of both strong selection and habitat choice. An increase in F(ST) for undifferentiated AFLPs between morphs, relative to within-morph comparisons, is consistent with there being a general barrier to gene flow across the contact zone. These features are consistent either with an episode of allopatric divergence followed by secondary contact or with primary, nonallopatric divergence. Further data will be needed to distinguish between these alternatives.     

Spatial mosaic and interfacial dynamics in a Müllerian mimicry system

Uncovering why spatial mosaics of mimetic morphs are maintained in a Müllerian mimicry system has been a challenging issue in evolutionary biology. In this article, we analyze the reaction diffusion system that describes two-species Müllerian mimicry in one- and two-dimensional habitats. Due to positive frequency-dependent selection, a local population first approaches the state where one of the comimicking patterns predominates, which is followed by slow movement of boundaries where different patterns meet. We then analyze the interfacial dynamics of the boundaries to find whether a stable cline is maintained and to obtain the wave speed if the cline is unstable. The results are: (1) In a spatially uniform habitat the morph with greater base fitness spreads both in one and two species system. (2) The strength of cross-species interaction determines whether the mimetic morph clines of model and mimic species coalesce into the same geographical region or pass through each other. The joint wave speed of clines decreases by increasing the number of comimicking species in the mimicry ring. (3) In spatial heterogeneous habitats, stable clines can be maintained due to the balance between the base fitness gradient and the biased gene flow by negative curvature of boundary. This allows the persistence of a spatial mosaic even if one of the morphs is in every place advantageous over the other. A balanced cline is also maintained if there is a gradient in the population density. (4) A new advantageous morph occurring at a local region is doomed to go to extinction in a finite time if the "radius" of initial distribution is below a threshold. Possible applications to the heliconiine butterfly mimicry ring, heterozygous disadvantage systems of chromosomal rearrangement and hybrid zone, the third phase of Wright's Shifting Balance theory, and cytoplasmic incompatibility are discussed.     

Floral display size and spatial distribution of potential mates affect pollen deposition and female reproductive success in distylous Pulmonaria officinalis (Boraginaceae)

In animal‐pollinated plants, both the spatial distribution of flowering individuals and the number of flowers that an individual displays affect pollen deposition rates and female reproductive success. Heterostylous species are likely to be particularly sensitive to the contingencies of spatial distribution, as they are reproductively subdivided into distinct mating groups, which usually exhibit self‐ and intra‐morph incompatibility and differ in floral morphology. In this paper, we explore the joint effects of both spatial distribution of potential mates and floral display size on morph‐specific pollen deposition rates and seed set patterns in two natural populations of Pulmonaria officinalis, a distylous species with a weak self‐incompatibility system. Both total stigmatic pollen load and the proportion of legitimate pollen decreased with increasing spatial isolation. Legitimate (intermorph) pollen transfer was, however, asymmetric and decreased more rapidly with decreasing proximity to a compatible legitimate mating partner in the S‐morph than in the L‐morph. Total stigmatic pollen loads per flower increased with increasing floral display size, indicating that large plants are disproportionately more visited than smaller individuals. However, because legitimate pollen deposition decreased with increasing floral display size, these results also suggest that larger numbers of flowers increase the degree of geitonogamous pollination. In both the L‐ and S‐morph, seed set significantly decreased with increasing isolation from a legitimate mating partner, but in the L‐morph seed set was less dependent on the spatial distribution of the S‐morph. In addition, seed set significantly increased with floral display size in the L‐morph, but not in the S‐morph. These findings indicate that the spatial distribution of potential mates and variation in floral display size may cause morph‐specific differences in pollen deposition rates and female reproductive success.     

SHELL STRENGTH OF COLOUR MORPHS OF THE MANGROVE SNAIL LITTORARIA PALLESCENS

The load required to break shells of the snail Littor-aria pallescens(Philippi) (Gastropoda: Littorinidae) has been established.Mass increases more than proportionally with size. Size forsize, relatively heavy shells are thicker than relatively lightones, and the thicker shells are stronger. Three samples fromdifferent localities differ significantly in strength. Littorariapallescens is polymorphic for shell colour. It is shown thatin two of the three samples, both from Papua New Guinea, individualsof the dark morph are significantly heavier and stronger thanthose of the yellow morph, while there is no difference betweenmorphs in the third sample, from Thailand. In the sample withthe most robust shells the dark individuals are stronger, massfor mass, than yellows. Thus, colour morph is sometimes, butnot always, associated with differences in shell characteristicswhich are likely to affect fitness. Where there is a difference,the dark morph is estimated to be on average about 22% strongerthan the yellow morph. The difference between morphs is smallcompared with the large variation in shell characters associatedwith size. (Received 20 May 1992; accepted 22 June 1992)     

A morph-ratio cline for keel petal colour in Lotus corniculatus L. along the north coastof Scotland

Summary

A survey of the relative frequencies of the dark and light keel variants of Lotus corniculatus L. was conducted in early July 1981, over 18 different sites located along the north coast of Scotland. Half of the sites surveyed were resampled in late July/early August 1984,to check for constancy of morph frequencies. The frequency of the dark keel morph recorded in 1981 showed a gradual increase from a value of 23% at Sheigra in the west to 87% at Duncansby Head in the east. Morph frequencies at sites sampled in 1981 and 1984 were highly correlated, and it was established that the change in dark keel frequency over eight of the sites surveyed in 1981 was significantly associated with parallel changes in mean annual rainfall and temperature. It is suggested that an experimental analysis of the morph-ratio cline for keel colour along the north coast of Scotland would aid our understanding of the factors which determine the distribution of the two keel colour morphs in Britain.     

Clinal variation in morphology and assortative mating in the soldier beetle, Chauliognathus pennsylvanicus (Goleoptera: Cantharidae)

In north Georgia populations of the soldier beetle, Chauliognathus pennsylvanicus , the length of the elytral spot varies clinally. At the southern end of a 200 km cline the distribution of spot length is unimodal with longer spot lengths predominating while at the northern end of the cline the distribution is bimodal but with shorter spot lengths being more frequent. North of the cline only short elytral spot lengths are observed, while the converse is true south of the cline. The strength of assortative mating on the basis of elytral spot length increases from south to north along the cline, resulting in complete pre-mating isolation between short and long spot length morphs at the north end of the cline. Laboratory mate choice tests indicate that assortative mating in the field is not the result of differential timing of activity or microhabitat choice but rather that it represents a real behavioural preference. Individuals from monomorphic populations on either side of the cline do not mate assortatively in the laboratory, indicating that reproductive isolation has evolved on the cline.     

Molecular phylogeny of Elephantidae. Extreme divergence of the extant forest African elephant.

A phylogenetic study of the Elephantidae (Proboscidea, Mammalia) is based on the cytochrome b mitochondrial gene: 31 terminals, that is, all known sequences, one non-elephantid proboscidean, the extinct American mastodon, and four outgroups. The data set includes 11 new sequences with the first published sequence of the forest African elephant, L. a. cyclotis. The analyses of extant taxa only and of both extant and extinct taxa show that L. a. cyclotis is highly divergent from L. a. africana. It is as divergent from L. a. africana as Loxodonta is divergent from Elephas. Southern L. a. africana form a clade. The continental subspecies E. m. indicus is paraphyletic with individuals from India and Thailand closer to E. m. maximus (Sri-Lanka). Members of Mammuthus primigenius are more closely related to Loxodonta although they do not form a clade; two specimens of M. primigenius are closer to L. a. africana making the genus Loxodonta paraphyletic. The latter conclusion may be partly due to unequal length of the various polymorphic mammoth sequences.     

Differentiation in a geographical mosaic of plants coevolving with ants: phylogeny of the Leonardoxa africana complex (Fabaceae: Caesalpinioideae) using amplified fragment length polymorphism markers

Comprising four allopatric subspecies that exhibit various grades of ant-plant interactions, from diffuse to obligate and symbiotic associations, the Leonardoxa africana complex (Fabaceae, Caesalpinioideae) provides a good opportunity to investigate the evolutionary history of ant-plant mutualisms. A previous study of the L. africana complex based on chloroplast DNA noncoding sequences revealed a lack of congruence between clades suggested by morphological and plastid characters. In this study, we analysed phylogenetic relationships within the L. africana complex using a Bayesian probability approach on amplified fragment length polymorphism markers. The results reported permit partial validation of the four subspecies of L. africana previously defined by morphological and ecological markers. Incongruences between phylogenies based on chloroplast DNA and amplified fragment length polymorphism markers are discussed in the light of morphological and ecological data, and confronted with hypotheses of convergence, lineage sorting and introgression.     

Geographical variations of elytral color polymorphism in Cheilomenes sexmaculata (Fabricius) (Coleoptera: Coccinellidae)

The geographical variation in elytral color polymorphism in Cheilomenes sexmaculata (Fabricius) was analyzed based on data from specimen surveys. In all, 1549 individuals collected from different latitudes throughout Indonesia to Japan were categorized into 20 morph types of elytra. Results show that the morph types have a geographical cline: dark types increased with latitude, although the light types showed higher relative frequency in lower latitudes, which suggests that the geographic variation in elytral color polymorphism in C. sexmaculata is a product of selection by climate. The darker morph types might be advantageously able to make fuller use of insolation at higher latitudes, whereas the lighter morph types were likely to reduce heat stress at lower latitudes. In most areas across Southeast and South Asia, all specimens were of the lightest type, which may imply either: (i) the saturation of genes expressing light morph types, which have less solar absorption, due to tropical climate; or (ii) an enhanced warning function of bright red against predators. On Miyako Island of Japan, a unique frequency of morph types was found compared to the adjacent areas.     

Nymphal colour/pattern polymorphism in the leafhoppers Eupteryx urticae (F.) and E. cyclops Matsumura (Hemiptera: Auchenorrhyncha): spatial and temporal variation in morph frequencies

Variation in colour/pattern morph frequencies in Eupteryx urticae and E. cyclops is described for various field populations. Eupteryx urticae populations in S Wales exhibit a steep morph-ratio cline, such that black morph frequencies are positively correlated with altitude. High melanic frequencies at high-altitude sites, and the absence of the two darker morphs in lowland populations, suggest a similar trend in E. cyclops , but the data are insufficient to confirm this statistically. No differences in morph frequencies were detected on different parts of the primary host plant or on alternative host species. Similarly, there were no consistent trends within or between the two annual generations of either species, although melanic morph frequencies in one E. urticae population were heterogeneous over 10 generations. It is suggested that the polymorphism in E. urticae is strongly influenced by climate selection, darker morphs being at an advantage in cooler environments where their coloration enhances absorption of solar radiation. The advantage gained through thermal melanism is probably balanced by visual selection against black morphs by entomophagous parasitoids.     

Citizen science reveals unexpected continental-scale evolutionary change in a model organism

Organisms provide some of the most sensitive indicators of climate change and evolutionary responses are becoming apparent in species with short generation times. Large datasets on genetic polymorphism that can provide an historical benchmark against which to test for recent evolutionary responses are very rare, but an exception is found in the brown-lipped banded snail (Cepaea nemoralis). This species is sensitive to its thermal environment and exhibits several polymorphisms of shell colour and banding pattern affecting shell albedo in the majority of populations within its native range in Europe. We tested for evolutionary changes in shell albedo that might have been driven by the warming of the climate in Europe over the last half century by compiling an historical dataset for 6,515 native populations of C. nemoralis and comparing this with new data on nearly 3,000 populations. The new data were sampled mainly in 2009 through the Evolution MegaLab, a citizen science project that engaged thousands of volunteers in 15 countries throughout Europe in the biggest such exercise ever undertaken. A known geographic cline in the frequency of the colour phenotype with the highest albedo (yellow) was shown to have persisted and a difference in colour frequency between woodland and more open habitats was confirmed, but there was no general increase in the frequency of yellow shells. This may have been because snails adapted to a warming climate through behavioural thermoregulation. By contrast, we detected an unexpected decrease in the frequency of Unbanded shells and an increase in the Mid-banded morph. Neither of these evolutionary changes appears to be a direct response to climate change, indicating that the influence of other selective agents, possibly related to changing predation pressure and habitat change with effects on micro-climate.