Ten years ago, Joseph Felsenstein (35) and I (56) both wrote reviews discussing the maintenance of genetic polymorphisms in heterogeneous environments. I addressed the question of the importance in maintaining genetic variation of diversifying selection (sometimes called the niche-variation hypothesis), i.e. selection for different alleles in different environments. My focus was on the evidence and theory supporting the connection of a variable environment with genetic variation, particularly as an explanation for the large amounts of allozymic variation. At that time, the empirical evidence suggesting a genetic-environment connection for allozymic variation was mostly correlative and not in general experimentally based. Theory suggested, however, that polymorphism maintenance was possible in a variable environment; it was most likely when there was variable selection in space and limited gene flow and/or habitat selection. The purpose of this review is to evaluate the research of the intervening decade on genetic polymorphism in variable environments. The topics of this review are divided in a fashion similar to that of the earlier review. First, I mention some recent work in which there has been detailed investigation of the relationship of different environments and the maintenance of genetic variation. Second, I review the theoretical developments in the past decade. Finally, I discuss recent experimental work in some detail. An emphasis in the review is to evaluate these experimental studies, a number of which were designed specifically to determine the importance of heterogeneous environments in maintaining genetic variation.

Genetic polymorphism in heterogeneous environments: a decade later

Because adaptive shifts may often be initiated by evolutionary changes in behavior, it is of interest to determine the extent to which natural populations harbor genetic variation for ecologically important behaviors. Habitat preference is an especially significant behavior, be- cause it determines the regime of natural selection acting on loci that affect adaptation to the environment. A survey of the literature reveals that genetic variation for habitat selection is common, especially in arthropods and mollusks, the groups that have been studied most fre- quently. Possible adaptive mechanisms by which this variation could be maintained within populations include a genetic correlation between density-independent fitness in a habitat and a preference for it; and soft selection, whereby density-dependent population regulation occurs independently in separate habitats. Several studies have documented a phenotypic correlation between preference and performance, but as yet, no such genetic correlations have been un- equivocally demonstrated. We show theoretically that under hard selection, optimal habitat selection may often lower the probability of maintaining a polymorphism at a locus that affects adaptation to different habitats. Soft selection appears much more likely to promote variation for habitat preference. Mechanisms including resource competition and natural enemies whose numbers build up in a habitat-specific manner in response to host or prey density have the capacity to bring about selection favoring alleles whose carriers prefer relatively underused habitats. We believe that more progress in understanding the evolution of habitat preference will come from studies of these ecological mechanisms than from further demonstrations of the mere existence of genetic variation for such preferences.

Genetic Variation for Habitat Preference: Evidence and Explanations

SUMMARY (1) The life history of the polymorphic land snail Arianta arbustorum was investigated in five natural populations along an altitudinal gradient from 1220 to 2600 m in the Swiss Alps. In order to assess the environmentally-induced variation of reproductive characters snails were transplanted to the lowlands. (2) Adult size decreased from 19-9 to 16-0 mm (mean shell breadth) with increasing altitude, age at maturity increased from 1-9 to 5-0 years, but median adult longevity and adult survival rates were approximately the same at all altitudes. (3) Clutch number, clutch size, egg size and reproductive investment per year decreased with increasing altitude in resident snails, whereas reproductive investment per egg increased. Within populations, clutch number, number of eggs produced per year and egg size scaled allometrically with shell size indicating a size-specific fecundity. (4) Transplanted snails laid 1-3-11-5 times more clutches than did resident snails. However, no differences in clutch size, egg dry weight and hatching success were found between transplanted and resident snails, except in one population, in which transplanted snails laid smaller clutches with larger eggs and scored a lower hatching success. (5) Transplanted snails were less variable in reproductive characters than resident ones, except for hatching success. (6) In general, life-history characters did not appear to be correlated with shell or body colour. (7) Although proximate factors like temperature explain most of the variation in life history, evidence was obtained also for genetic divergence among populations. The results match the predictions of the adversity selection model well, rather than those of bet

Life history of the land snail arianta arbustorum along an altitudinal gradient

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.

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

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.

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A two–stage model for Cepaea polymorphism

The behaviour of morphs of Arianta arbustorum has been investigated using a new technique involving a paint which fades in daylight. The technique was used to study the response of different morphs to exposure to sunlight at a homogeneous woodland habitat and a heterogeneous open habitat. The yellow morph showed a significantly higher rate of fading than the brown morph. A mark, release and recapture programme was used to analyse the association between frequencies of different morphs recaptured and not recaptured. In both habitats, there was a general tendency for the frequency of recapture to increase with increasing age in both morphs. Habitat selection resulting from different behaviour of different morphs of A. arbustorum is discussed. Morph frequencies can be related to habitat, the brown morphs of A. arbustorum are significantly less frequent in the open habitat. The behavioural responses of Cepaea hortensis, present with A. arbustorum in two other populations, to the exposure of sunshine were also studied. Climatic selection by solar energy associated with different morphs, species and habitat are also discussed.

Difference in habitat selection by different morphs of the land snail Arianta arbustorum

The noctural activities of the phenotypic shell colour morphy and age classes (adults and juveniles) of Arianta arbustorum were recorded 1 day week-1 for 4 weeks in several laboratory microclimatic conditions. Six constant temperatures between 3 and 18dC and four levels of relative humidities between 34 and 98% were maintained. A light regime of 16 h light: 8 h dark was used. There are highly significant differences in activity at different levels of adaptation temperature and relative humidity. The interaction between these factors is significant. There are no significant differences in nocturnal activity between the two phenotypic shell colours nor between the two age classes, but the interaction between morph and relative humidity is significant. The interaction between age classes and relative humidity is also significant. Yellows are more active than browns at high humidities, but less active at low. They are therefore likely to be behaviourally more responsive than browns in an environment of fluctuating humidities. This result is discussed in relation to the maintenance of the polymorphism.

The effects of temperature and humidity on the nocturnal activity of different shell colour morphs of the land snail Arianta arbustorum

The mortality of phenotypic shell colour morphs and age classes of the snail Arianta arbustorum in several microclimatic conditions was recorded. An analysis of variance was performed on five factors: adaptation temperature, relative humidity, shell colour, age class and test temperature. There were no significant differences in the mortality between different adaptation temperatures or relative humidities, but the interaction of these two factors was highly significant. There were significant differences in mortality rate between test temperature and age class. The mortality of the brown morph was higher than the yellow one at all adaptation temperatures (overall, P < 0.05). There were no significant differences between the mortality rates of the two morphs at different relative humidities. The mortality of the brown morph was higher than that of the yellow at six out of seven test temperatures. Juvenile snails survived significantly better than adults at all test temperatures.

A. H. Abdel-Rehim

Papers

Difference in habitat selection by different morphs of the land snail Arianta arbustorum

The effects of temperature and humidity on the nocturnal activity of different shell colour morphs of the land snail Arianta arbustorum

Influence of shell colour on the mortality rate of the land snail Arianta arbustorum under different microclimatic regimes