An experimental test of the role of predators in the maintenance of a genetically based polymorphism

Polymorphisms provide one of the most useful tools for understanding the maintenance of genetic and phenotypic variation in nature. We have previously described a genetically based polymorphism in dorsal patterning that is expressed by female brown anole lizards, Anolis sagrei, which occur in Bar, Diamond and intermediate Diamond-Bar morphs. Previous studies of island populations in The Bahamas support a role for selection in maintaining the polymorphism, but the agents responsible for this selection remain unclear. We tested two main hypotheses regarding the importance of predation as a selective agent that maintains the polymorphism within populations. First, we tested whether correlational selection favours different combinations of morph, locomotor performance and escape behaviour by measuring morph-specific natural selection on sprint speed, running endurance and the propensity of females to either 'freeze' or 'run' in response to attempted capture. Morphs did not differ in any of these traits, nor did correlational selection consistently favour any particular combinations of morph and antipredator behaviour. Second, we experimentally excluded bird and snake predators from two entire island populations, allowed these predators access to two additional islands and then measured subsequent differences in natural selection on morphs in each population. Predators reduced the survival of Bar and Diamond females, but not of genetically intermediate Diamond-Bar females. These results provide limited evidence that predation may play a role in maintaining this polymorphism, although the functional traits that could account for differential susceptibility to predation remain unclear.     

Population structure and coil dimorphism in a tropical land snail

Tree snails of the subgenus Amphidromus s. str. are unusual because of the chiral dimorphism that exists in many species, with clockwise (dextrally) and counter-clockwise (sinistrally) coiled individuals co-occurring in the same population. Given that mating in snails is normally impeded when the two partners have opposite coil, positive frequency-dependent selection should prevent such dimorphism from persisting. We test the hypothesis that a strong population structure with little movement between tree-based demes may result in the fixation of coiling morphs at a very small spatial scale, but apparent dimorphism at all larger scales. To do so, we describe the spatial structure in a Malaysian population of A. inversus (Müller, 1774) with 36% dextrals. We marked almost 700 juvenile and adult snails in a piece of forest consisting of 92 separate trees, and recorded dispersal and the proportions of dextrals and sinistrals in all trees over a 7-day period. We observed frequent movement between trees (155 events), and found that no trees had snail populations with proportions of dextrals and sinistrals that were significantly different from random. Upon recapture 1 year later, almost two-thirds of the snails had moved away from their original tree. We conclude that population structure alone cannot stabilise the coil dimorphism in Amphidromus.     

Predation and the maintenance of color polymorphism in a habitat specialist squamate

Multiple studies have addressed the mechanisms maintaining polymorphism within a population. However, several examples exist where species inhabiting diverse habitats exhibit local population-specific polymorphism. Numerous explanations have been proposed for the maintenance of geographic variation in color patterns. For example, spatial variation in patterns of selection or limited gene flow can cause entire populations to become fixed for a single morph, resulting in separate populations of the same species exhibiting separate and distinct color morphs. The mottled rock rattlesnake (Crotalus lepidus lepidus) is a montane species that exhibits among-population color polymorphism that correlates with substrate color. Habitat substrate in the eastern part of its range is composed primarily of light colored limestone and snakes have light dorsal coloration, whereas in the western region the substrate is primarily dark and snakes exhibit dark dorsal coloration. We hypothesized that predation on high contrast color and blotched patterns maintain these distinct color morphs. To test this we performed a predation experiment in the wild by deploying model snakes at 12 sites evenly distributed within each of the two regions where the different morphs are found. We employed a 2×2 factorial design that included two color and two blotched treatments. Our results showed that models contrasting with substrate coloration suffered significantly more avian attacks relative to models mimicking substrates. Predation attempts on blotched models were similar in each substrate type. These results support the hypothesis that color pattern is maintained by selective predation.     

Differences in predatory pressure on terrestrial snails by birds and mammals

The evolution of shell polymorphism in terrestrial snails is a classic textbook example of the effect of natural selection in which avian and mammalian predation represents an important selective force on gene frequency. However, many questions about predation remain unclear, especially in the case of mammals. We collected 2000 specimens from eight terrestrial gastropod species to investigate the predation pressure exerted by birds and mice on snails. We found evidence of avian and mammalian predation in 26.5% and 36.8% of the shells. Both birds and mammals were selective with respect to snail species, size and morphs. Birds preferred the brown-lipped banded snail Cepaea nemoralis (L.) and mice preferred the burgundy snail Helix pomatia L. Mice avoided pink mid-banded C. nemoralis and preferred brown mid-banded morphs, which were neglected by birds. In contrast to mice, birds chose larger individuals. Significant differences in their predatory pressure can influence the evolution and maintenance of shell size and polymorphism of shell colouration in snails.     

Patterns of genetic diversity in the polymorphic ground snake (Sonora semiannulata)

We evaluated the genetic diversity of a snake species with color polymorphism to understand the evolutionary processes that drive genetic structure across a large geographic region. Specifically, we analyzed genetic structure of the highly polymorphic ground snake, Sonora semiannulata, (1) among populations, (2) among color morphs (3) at regional and local spatial scales, using an amplified fragment length polymorphism dataset and multiple population genetic analyses, including F_ST-based and clustering analytical techniques. Based upon these methods, we found that there was moderate to low genetic structure among populations. However, this diversity was not associated with geographic locality at either spatial scale. Similarly, we found no evidence for genetic divergence among color morphs at either spatial scale. These results suggest that despite dramatic color polymorphism, this phenotypic diversity is not a major driver of genetic diversity within or among populations of ground snakes. We suggest that there are two mechanisms that could explain existing genetic diversity in ground snakes: recent range expansion from a genetically diverse founder population and current or recent gene flow among populations. Our findings have further implications for the types of color polymorphism that may generate genetic diversity in snakes.     

Frequency-dependent predation and maintenance of prey polymorphism

In positive frequency-dependent predation, predation risk of an individual prey correlates positively with the frequency of that prey type. In a number of small-scale experiments individual predators have shown frequency-dependent behaviour, often leading to the conclusion that a population of such predators could maintain prey polymorphism. Using simulations, I studied the dynamics of frequency-dependent predation and prey polymorphism. The model suggests that persistence of prey polymorphism decreases with increasing number of predators that show frequency-dependent behaviour, questioning conclusions about polymorphism based on experiments with few predators. In addition, prey population size, prey crypsis, difference in crypsis between prey morphs and the way the behaviour was adjusted affected the persistence of polymorphism. Under some circumstances prey population remained polymorphic for a shorter time under frequency-dependent than under frequency-independent predation. This suggests that although positive frequency-dependent predator behaviour may maintain prey polymorphism, it is not a sufficient condition for persistent prey polymorphism.     

花柱卷曲性的维持及功能性别特化

花柱多态型的型比通过选型交配形成的负频率依赖的选择来维持。种群空间格局对于频率依赖选择所维持的花柱多态型是至关重要的。该研究使用摆放实验构建不同型比的马来良姜(Alpinia mutica)人工种群, 以评价花柱卷曲性促进选型交配的功能。使用邻域模型调查了云南草蔻(Alpinia blepharaocalyx)种群中的目标植株的坐果数、结籽数及其邻域中花序的数量和型偏以探讨在局域尺度上目标植株的雌性适合度是否受负频率依赖的选择。通过比较云南草蔻上举型和下垂型各繁殖性状的差异以及两型的功能性别的计算以评估两型功能性别可能存在的特化趋势。摆放实验结果说明花柱卷曲性形成的二型种群可以促进型间花粉传递。在局域尺度上, 云南草蔻两型倾向于同型聚集分布, 这一分布特点反映出其克隆生长特性。统计结果说明: 邻域中异型花粉供体相对丰富度对两型目标植株都无影响; 目标植株雌性适合度在邻域中不受负频率依赖选择的影响。这一结果并不支持负频率依赖的选择在该研究尺度上是影响种群型比结构的主要机制。云南草蔻两型个体在花期和果期的繁殖指标上不存在显著差异; 功能性别计算结果显示选型交配是种群内唯一的交配模式时, 下垂型功能性别偏雌性而上举型功能性别偏雄性。这一功能性别特化的趋势可能是通过对上举型的雄性功能的选择而造成的, 并可能与种群型结构相关。当功能性别计算只考虑自交而忽略近交衰退时, 种群功能性别偏向雌性。     

Colour polymorphism and thermal capacities in Theba pisana (O.F. Müller 1774)

Several land snail species are highly polymorphic regarding their shell colouration. This polymorphism has been related to predatory effects as well as climatic reasons, assuming that dark morphs benefit from being more cryptic and therefore less prone to predation, whereas pale morphs are at an advantage under solar radiation, as they are suspected to heat up less. However, the assumption of different thermal capacities of these morphs is based on experiments with little standardisation or little environmental relevance. In this study, we aimed at measuring thermal capacities of two different morphs (pale versus dark-brown banded) of the Mediterranean land snail Theba pisana, applying a standardised and environmentally relevant test set-up, in order to prove whether darker morphs indeed do heat up more than lighter coloured morphs. We did not find any differences in the thermal capacity of the different morphs and conclude that thermal capacity of the shell is predominantly defined by its material rather than its coloration. These results are discussed with regard to previous studies on thermal characteristics of different land snail morphs and correlations between climate and morph distribution.     

Differential predation on sexes affects colour polymorphism of the isopod Idotea baltica (Pallas)

Variable selection, including spatio-temporal variation, frequency-dependent selection and differential selection due to habitat choice, may maintain polymorphism in heterogeneous environments. We studied predation as a selective agent on colour polymorphism of the aquatic isopod I baltica. Variable predation on this species can arise from at least three sources. First, apostatic selection was studied by testing the formation of preferences on colour morphs in the perch, a common predator of I baltica. Such acquired preferences should induce apostatic selection. While our results indicate some acquired preferences, there was significant heterogeneity in the behaviour of predator individuals. Second, temporal variation in selection can arise due to habitat shift from the green algae juvenile habitat to the bladderwrack adult habitat, and the consequent change in the crypsis of the morphs. Different crypsis between sexes probably promoted high predation mortality among females in the juvenile habitat. The high rate of male mortality during the breeding period, on the other hand, was presumably due to their high mate-searching activity. Third, the sex-dependent habitat choice of I baltica leads to sexual differences in the susceptibility of morphs to predation. Predators preferred the white-spotted morph over the uniform one in males but not in females, supporting the 'dimorphic niche' hypothesis as an explanation of sexual differences in morph frequencies. Finally, no evidence was found that the colouration patterns were under sexual selection. We therefore conclude diat variable predation is the most promising explanation for the maintenance of polymorphism in I. baltica.     

Direct and indirect selection on floral pigmentation by pollinators and seed predators in a color polymorphic South African shrub

The coexistence of different color morphs is often attributed to variable selection pressures across space, time, morph frequencies, or selection agents, but the routes by which each morph is favored are rarely identified. In this study we investigated factors that influence floral color polymorphisms on a local scale in Protea, within which approximately 40% of species are polymorphic. Previous work shows that seed predators and reproductive differences likely contribute to maintaining polymorphism in four Protea species. We explored whether selection acts directly or indirectly on floral color in two populations of Protea aurea, using path analysis of pollinator behavior, nectar production, seed predation, color, morphology, and maternal fecundity fitness components. We found that avian pollinators spent more time on white morphs, likely due to nectar differences, but that this had no apparent consequences for fecundity. Instead, the number of flowers per inflorescence underpinned many of the reproductively important differences between color morphs. White morphs had more flowers per inflorescence, which itself was positively correlated with nectar production, seed predator occurrence, and total long-term seed production. The number of seeds per plant to survive predation, in contrast, was not directly associated with color or any other floral trait. Thus, although color differences may be associated with conflicting selection pressures, the selection appears to be associated with the number of flowers per inflorescence and its unmeasured correlates, rather than with inflorescence color itself.     

Opposing fitness consequences of colour pattern in male and female snakes

Local populations of the adder, Vipera berus, are polymorphic for dorsal colour pattern, containing both melanistic (black) and zig-zag patterned individuals. Colour patterns in snakes influence crypsis and thermoregulatory capacity and therefore may be subjected to natural selection. To find an explanation for the maintenance of this polymorphism I examined temporal and spatial variation in morph frequency, and tested for differential selection among morphs using data from a six year capture-mark-recapture study. The data derive from six groups of islands in the Baltic Sea off the Swedish east coast, two mainland localities near the coast, and one inland locality. Morph frequency did not change over time within a population but varied among populations: melanistic individuals were not found at the inland locality, but comprised from 17 to 62% of the coastal and island populations. Adders frequently moved between islands within a group, but the tendency to disperse was independent of morph. These results suggest that the polymorphism is stable and maintained by a deterministic process. Scar frequency was twice as high among melanistic as among zig-zag snakes, and melanistic individuals were easier to capture, indicating that predation may be higher on the melanistic morph. Colour morphs did not differ in body size, but analysis of recapture data shows evidence for differential survival among morphs. Zig-zag males survived better than melanistic males, but the relative survival rates of morphs were reversed in females. This difference was consistent through time and may be due to sexual differences in behaviour, with melanism increasing predation intensity when associated with male but not with female behaviour. Opposing fitness consequences of colour pattern in the two sexes may help maintain colour polymorphism within populations of Vipera berus.     

Frequency-dependent variation in reproductive success in Narcissus: implications for the maintenance of stigma-height dimorphism

Negative frequency-dependent selection is a major selective force maintaining sexual polymorphisms. However, empirical demonstrations of frequency-dependent reproductive success are rare, particularly in plants. We investigate this problem by manipulating the frequencies of style morphs in a natural population of Narcissus assoanus, a self-incompatible herb with style-length dimorphism and intra-morph compatibility. We predicted that the reproductive success of morphs would vary negatively with their frequency because of the effects of morph-specific differences in sex-organ position on patterns of pollen transfer. This prediction was generally supported. The fruit and seed set of the two morphs did not differ significantly in plots with 1 : 1 morph ratios. However, short-styled plants produced significantly fewer seeds than long-styled plants in monomorphic plots, and significantly more seeds than long-styled plants in plots with 'long-biased' morph ratios. These patterns indicate that in the absence of physiological barriers to intra-morph mating, negative frequency-dependent selection contributes to the maintenance of stylar polymorphism through inter-morph pollen transfer. Our experimental results also provide insights into the mechanisms governing the biased style-morph ratios in populations of Narcissus species.     

The adaptive significance of colour pattern polymorphism in the Australian scincid lizard Lampropholis delicata

Females of Lampropholis delicata are dimorphic for colour pattern, the difference between morphs being the presence or absence of a distinct white mid-lateral stripe. A less distinct striped morph occurs also in males. We evaluated alternative hypotheses for the maintenance of this polymorphism by examining temporal and spatial variation in morph frequency, testing for differential selection among morphs using data on body size and reproductive traits from preserved specimens, and experimentally manipulating colour pattern in free-ranging lizards of both sexes, to assess the influence of the lateral stripe on survival rates. We found that the relative frequency of striped individuals varied among populations and decreased from north to south in both sexes, coincident with an increasing incidence of regenerated tails. Morph frequencies did not change through time within a population. Striped gravid females appeared to survive better and produced larger clutches than did non-striped females. In our experimental study, the relationship between survival and colour morph differed between the two sexes; males painted with a white lateral stripe had lower survival than control (brown stripe) males, but survival did not differ between striped and control females. The different response in the two sexes may be due partly to differences in temperature and microhabitat selection. We propose that the white lateral stripe decreases susceptibility to predators in gravid females but increases risk of predation in males, especially in combination with low temperatures. The polymorphism might be maintained by: (1) opposing fitness consequences of the stripe in males and females; (2) sex-specific habitat selection; and (3) gene flow in combination with spatial variation in relative fitness of the two morphs.     

GEOGRAPHIC VARIATION, FREQUENCY-DEPENDENT SELECTION, AND THE MAINTENANCE OF A FEMALE-LIMITED POLYMORPHISM

A central problem in evolutionary biology is to understand how spatial and temporal variation in selection maintain genetic variation within and among populations. Brown anole lizards ( Anolis sagrei ) exhibit a dorsal pattern polymorphism that is expressed only in females, which occur in "diamond,""bar," and intermediate "diamond-bar" morphs. To understand the inheritance of this polymorphism, we conducted a captive breeding study that refuted several single-locus models and supported a two-locus mode of inheritance. To describe geographic variation in morph frequencies, we surveyed 13 populations from two major islands in The Bahamas. Morph frequencies differed substantially between major islands but were highly congruent within each island. Finally, we measured viability selection on each island to test two hypotheses regarding the maintenance of the polymorphism: (1) that spatial variation in selection maintains variation in morph frequencies between islands, and (2) that temporal variation in selection across years maintains variation within islands. Although bar females had relatively lower survival where they were rare, our data do not otherwise suggest that selection varies spatially between islands. However, diamond-bar females were subject to positive frequency-dependent selection across years, and the relative fitness of bar and diamond females alternated across years. We propose that this polymorphism is maintained by temporal variation in selection coupled with the sheltering of alleles via a two-locus inheritance pattern and sex-limited expression.     

Spatial ecology of mating success in a sexually polymorphic plant

The spatial context of reproduction is of crucial importance to plants because of their sessile habit. Since pollen and seed dispersal is often restricted, mating success is likely to depend on the quantity and quality of mates in local neighbourhoods. Here we use neighbourhood models to investigate the spatial ecology of pollination and mating in Narcissus assoanus, a sexually polymorphic plant with two mating morphs that differ in style length. By mapping individuals in eight populations from southwestern France, we investigated the influence of the density and morph identity of plants at different spatial scales on variation in female fertility. By using inferences on the expected patterns of pollen transfer based on floral morphology, we were able to predict the quantitative relations between local morph ratios and variation in fertility. Our analyses revealed differences in the spatial clustering of morphs and in their response to plant density and morph identity within local neighbourhoods. Mating success in N. assoanus was characterized by both density- and frequency-dependent processes, a condition that may be a general feature of the spatial ecology of plant mating.     

A two-stage model for Cepaea polymorphism

The history of the study of snails in the genus Cepaea is briefly outlined. Cepaea nemoralis and C. hortensis are polymorphic for genetically controlled shell colour and banding, which has been the main interest of the work covered. Random drift, selective predation and climatic selection, both at a macro- and micro-scale, all affect gene frequency. The usual approach to understanding maintenance of the polymorphism, has been to look for centripetal effects on frequency. Possible processes include balance of mutation pressure and drift, heterozygote advantage, relational balance heterosis, frequency-dependent predation, multi-niche selective balance, or some combination of these. Mutational balance is overlaid by more substantial forces. There is some evidence for heterosis. Predation by birds may protect the polymorphism, and act apostatically to favour distinct morphs. Although not substantiated for Cepaea, many studies show that predators behave in the appropriate manner, while shell colour polymorphisms in molluscs occur most commonly in species exposed to visually searching predators. It is not known whether different thermal properties of the shells help to generate equilibria. Migration between colonies is probably greater than originally thought. The present geographical range has been occupied for less than 5000 generations. Climatic and human modification alter snail habitats relatively rapidly, which in turn changes selection pressures. A simple simulation shows that migration coupled with selection which fluctuates but is not centripetal, may retain polymorphism for sufficiently long to account for the patterns we see today. There may therefore be a two-stage basis to the polymorphism, comprising long-term but weak balancing forces coupled with fluctuating selection which does not necessarily balance but results in very slow elimination. Persistence of genetic variants in this way may provide the conditions for evolution of a balanced genome.     

Polymorphic snails on varied backgrounds

The general matching of shell colours to background colours seen in terrestrial gastropods implies that, as in insects, visual predation is an important factor which has a long term directional effect. Polymorphism in snails is associated with background heterogeneity, but the causal relation of polymorphism to heterogeneity is not obvious. Predation could maintain polymorphism if predators are frequency dependent in their choice of prey. However, the appropriate predator behaviour does not depend directly on background heterogeneity. An indirect contribution could be that the heterogeneity serves to lower the signal:noise ratio during the predation process. Background heterogeneity could have a direct effect if the background provided specific elements mimicked by the morphs. The remaining diversity could aid the process by lowering the signal:noise ratio. Polymorphism could be maintained if there was frequency-dependent niche selection on the part of prey. Background diversity would then be directly involved. It is necessary that there should be independent control of numbers in the different niches. In warm conditions the niche selection could come about because darker morphs, which gain more radiant heat than paler ones, will move to more cryptic sites by seeking the shade. For morph frequences to approach equilibrium values closely it is necessary for the alleles controlling the polymorphism to exhibit dominance. Differences in received energy could make pale morphs disadvantageous compared with dark ones at low temperatures but advantageous at high ones. In spatially varied temperature conditions a polymorphism could be generated without predation. Density-dependent selection is again required.     

Speciation and gene flow between snails of opposite chirality

Left-right asymmetry in snails is intriguing because individuals of opposite chirality are either unable to mate or can only mate with difficulty, so could be reproductively isolated from each other. We have therefore investigated chiral evolution in the Japanese land snail genus Euhadra to understand whether changes in chirality have promoted speciation. In particular, we aimed to understand the effect of the maternal inheritance of chirality on reproductive isolation and gene flow. We found that the mitochondrial DNA phylogeny of Euhadra is consistent with a single, relatively ancient evolution of sinistral species and suggests either recent “single-gene speciation” or gene flow between chiral morphs that are unable to mate. To clarify the conditions under which new chiral morphs might evolve and whether single-gene speciation can occur, we developed a mathematical model that is relevant to any maternal-effect gene. The model shows that reproductive character displacement can promote the evolution of new chiral morphs, tending to counteract the positive frequency-dependent selection that would otherwise drive the more common chiral morph to fixation. This therefore suggests a general mechanism as to how chiral variation arises in snails. In populations that contain both chiral morphs, two different situations are then possible. In the first, gene flow is substantial between morphs even without interchiral mating, because of the maternal inheritance of chirality. In the second, reproductive isolation is possible but unstable, and will also lead to gene flow if intrachiral matings occasionally produce offspring with the opposite chirality. Together, the results imply that speciation by chiral reversal is only meaningful in the context of a complex biogeographical process, and so must usually involve other factors. In order to understand the roles of reproductive character displacement and gene flow in the chiral evolution of Euhadra, it will be necessary to investigate populations in which both chiral morphs coexist.     

The effect of coil phenotypes and genotypes on the fecundity and viability of Partula suturalis and Lymnaea stagnalis: implications for the evolution of sinistral snails

Why are sinistral snails so rare? Two main hypotheses are that selection acts against the establishment of new coiling morphs, because dextral and sinistral snails have trouble mating, or else a developmental constraint prevents the establishment of sinistrals. We therefore used an isolate of the snail Lymnaea stagnalis, in which sinistrals are rare, and populations of Partula suturalis, in which sinistrals are common, as well as a mathematical model, to understand the circumstances by which new morphs evolve. The main finding is that the sinistral genotype is associated with reduced egg viability in L. stagnalis, but in P. suturalis individuals of sinistral and dextral genotype appear equally fecund, implying a lack of a constraint. As positive frequency‐dependent selection against the rare chiral morph in P. suturalis also operates over a narrow range (< 3%), the results suggest a model for chiral evolution in snails in which weak positive frequency‐dependent selection may be overcome by a negative frequency‐dependent selection, such as reproductive character displacement. In snails, there is not always a developmental constraint. As the direction of cleavage, and thus the directional asymmetry of the entire body, does not generally vary in other Spiralia (annelids, echiurans, vestimentiferans, sipunculids and nemerteans), it remains an open question as to whether this is because of a constraint and/or because most taxa do not have a conspicuous external asymmetry (like a shell) upon which selection can act.     

Ecological divergence among sympatric colour morphs in blood pythons, Python brongersmai

Blood pythons in northeastern Sumatra display a series of discrete colour morphs, even among hatchlings within a single clutch. The first step towards understanding the maintenance of this polymorphism is to test the null hypothesis that colour variation in this species has no major biological correlates. Data on >2,000 blood pythons killed for the commercial leather industry enabled us to test, and reject, this hypothesis. The four colour morphs differed significantly in most of the traits that we measured, including temporal and spatial abundances, sex ratios, age structures, mean adult body sizes, body shapes (tail length and body mass relative to snout-vent length), energy stores, numbers of gut parasites, prey types, feeding frequencies and clutch sizes. The causal basis for these associations remains unclear, but is likely to involve three processes: direct effects of colour, linkages between genes for colour and other traits, and correlated spatial heterogeneity in colour, morphology and ecology. The colour polymorphism may be maintained by frequency-dependent selection and genotype-specific habitat selection, because these sedentary ambush predators are under strong selection for effective camouflage to hide them from both predators and potential prey. In support of this hypothesis, similar colour polymorphisms have evolved independently in several other snake taxa that rely upon ambush predation. Received: 18 December 1997 / Accepted: 23 March 1998