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Keywords:

  • climate;
  • DNA decay;
  • pleiotropy;
  • specialist

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES

Many insects are climate specialists – restricted to a narrow range of latitudes, humidity conditions and/or altitudes. Yet there are also numerous climate generalists, whose distribution might span from the tropics to temperate areas. Comparisons of related insect species normally indicate that the resistance of species to climatic extremes and reproductive output under different climatic conditions match expectations based on their distributions. Yet these patterns do not ultimately explain why climate specialists and generalists have evolved over time. Three evolutionary hypotheses that are invoked to explain climate specialisation are (1) constraints arising from antagonistic pleiotropy (costs); (2) DNA decay due to mutational processes; and (3) the difficulty of adapting due to the requirement of multidimensional changes or because of gene flow. Here I outline these hypotheses, and consider predictions and supporting evidence from several sources including polymorphism studies, quantitative genetic studies, species comparisons and genomic comparisons. All three explanations are likely to contribute to climate specialisation and the DNA decay/multidimensional adaptation hypotheses deserve more consideration.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES

Climate can limit distributions of insects directly by influencing survival and fecundity, or indirectly through effects on interacting species, including species that act as food sources, natural enemies or competitors (Gaston 2003). Direct effects of climate have been documented on numerous occasions, particularly in the context of cool conditions experienced at high latitudes/altitudes where the effectiveness of herbivorous, predatory and parasitic insects on host insect populations often decreases sharply due to stressful conditions (Hodkinson 1999). Range limits are often driven by a combination of host plants/animals and climatic factors, and predictions about likely shifts in distribution under climate change need to consider both factors (Hellmann et al. 2008; Merrill et al. 2008; Terblanche et al. 2008) within the context of local topographical variation (Hodkinson 2005). When particular groups of related insects are considered, many can be divided into specialists and generalists on the grounds of their climatic distributions (e.g. Andrew & Hughes 2005; Rohan et al. 2007). Closely related insects can differ markedly in their survival of climatic stresses as well as in their ability to reproduce and expand under different thermal conditions, influencing species distributions and abundance (Hellmann et al. 2008; Kellermann et al. 2009).

Because geographical and local distributions of insects often depend on climatic conditions, global warming is expected to shift species ranges and alter the dynamics of insect populations. Range shifts are most evident so far in expansions of warm-adapted species at cool upper latitude margins of ranges (Parmesan et al. 2005), and in outbreaks of pest organisms as warmer conditions expand pest distributions and increase their population size (Jepsen et al. 2008). Conversely, an increased incidence of hot and arid conditions is decreasing populations of some insects. Some herbivores have become locally extinct under hot conditions even when their host plants recover (Piessens et al. 2009) while insect parasitoids that help control herbivorous pests have become less common and effective as drier conditions have developed (Stireman et al. 2005). Locally, outbreaks of some migratory pests may be decreasing as a consequence of drier inland conditions (Hoffmann et al. 2008).

The responses of insect populations to climate change can be modified through evolution. In insects evolutionary shifts have occurred in the past few decades (Bradshaw & Holzapfel 2007; Hoffmann & Willi 2008) and are helping populations to exploit newly favourable conditions (Bradshaw & Holzapfel 2007). There is an enormous potential for such shifts in insects and invertebrates generally as indicated by a wealth of evidence for geographic variation in the responses of populations to climatic variation due to a history of selection and evolution (e.g. Hoffmann et al. 2003b; Shufran et al. 2004) as well as the results of experimental manipulations that suggest rapid evolutionary responses (Archer et al. 2007; Harmon et al. 2009; Van Doorslaer et al. 2009). Yet there are clearly limits to the extent that species can adapt to different climatic conditions through evolution. If there were no limits, a few rapidly evolving species might predominate across different climatic regions, whereas in practice climate restricts the invasibility of environments by arthropods (e.g. Arndt & Perner 2008).

In this overview I explore the different evolutionary hypotheses that have been proposed to understand the evolution of climate specialists and generalists. I consider evidence for the different hypotheses at the levels of populations and species, and the types of genetic signatures that might reflect past evolutionary processes leading to climatic specialisation. Data and models to test these hypotheses can help provide an understanding of why much of biodiversity is tied up with climate specialists with restricted distributions.

PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES

There are three main hypotheses about limits acting on specialist species. The first concerns trade-offs or more specifically antagonistic pleiotropy; alleles that increase resistance to high temperatures (or arid conditions) are expected to decrease performance at mild or low temperatures (or more humid conditions). At the phenotypic level, such alleles lead to trade-offs and a switch in the relative fitness of genotypes between environments. Specialists have an advantage over generalist species (or specialists adapted to different environmental conditions) because they can outperform them in a narrow set of conditions. This is the so-called ‘jack-of-all-trades is a master of none’ hypothesis and requires a genetically based cost of generalisation (Huey & Kingsolver 1989; Gilchrist 1995). Switching from a generalist to a specialist strategy is assumed to have some cost – the ability to exploit one resource efficiently is assumed to have a cost for exploiting a different resource. These costs can be built into ecological models of resource exploitation to predict the number and evolution of specialist species in an environment (Ma & Levin 2006). In terms of thermal response curves, costs assume that increased performance at one end of the response curve (thermal maximum or minimum) has some cost elsewhere, either at the opposite extreme or in terms of a reduction in optimal performance (Angilletta 2009).

The second hypothesis is associated with a loss of function: when a trait is no longer under selection, mutations accumulate and ensure that there is DNA decay in genes that are associated with that function. The eventual outcome is the loss of genetic variation and the loss of an ability to evolve in a particular direction at some future time point. This hypothesis has often been invoked to explain the evolution of specialisation and loss of function in microbes (Maughan et al. 2007; Hall & Colegrave 2008) and digital organisms (Ostrowski et al. 2007). It requires a rapid deterioration of adaptive potential to novel environments, due to the accumulation of mutations within structural and/or regulatory genes that are no longer under selection, such as the accumulation of stop codons in structural genes leading to truncated and non-functional protein products. The loss of function occurs because there is no longer any selection on genes controlling that function under the environmental conditions being experienced by an organism. However, if the environment then changes subsequently, the loss of function means that the species is unable to mount an adaptive response; it has effectively become specialised to an environment from its past history. Under this model of specialisation, it is assumed that species do not occur in all areas where they might once have been able to exist, i.e. the realised niche of an insect is assumed to be narrower than its potential niche at some point in its history. This is certainly the case for many species (e.g. Kimball et al. 2004; Fitzgerald et al. 2005; Roldan-Carrillo et al. 2005; Larsen & Sand-Jensen 2006). There are numerous reasons why the climatic conditions to which species are exposed might become narrow; a species might become restricted to an island or an area bounded by mountains, or because its host plants/animals contract in range.

In practice, the hypothesis of DNA decay can be difficult to distinguish from that of antagonistic pleiotropy because both hypotheses lead to apparent trade-offs when the performance of species is compared across environments (Presloid et al. 2008). The accumulation of mutations decreases fitness in an environment where a species is no longer found because selection is no longer removing mutations that have deleterious effects in that environment. Antagonistic pleiotropy also decreases fitness in an environment where a species is not found, but for a different reason. In this case alleles with a high fitness in the environment where the species occurs are predicted to act antagonistically on fitness in another environment where the species might not currently occur.

The third hypothesis is that climatic specialisation occurs because it is difficult to adapt to a different set of conditions, either in the face of the multidimensionality of adaptive changes required to obtain a selection response or in the face of gene flow. Under multidimensionality, individual components of evolutionary change might be possible, but adapting to new climatic conditions is difficult simply because of the large number of independent changes required in individual components for adaptation to be successful (Wagner 1988; Orr 2000). One way of thinking about this hypothesis is to consider the numbers of changes required for adapting to different thermal conditions. A cell might contain 104 different proteins, which are involved in 105 interactions that all can be sensitive to changes in temperature (Clarke 2003). If alternate forms of these proteins with different thermal sensitivities are segregating in populations, a very large number of evolutionary changes might be required to maintain optimal metabolic functioning under a new set of conditions. Adapting to new climatic conditions can also require a large number of changes in sensing and dealing with a new set of stressful conditions as well as shifting metabolic optima. When there are genetic correlations among the multiple traits under selection, adaptive responses become even more difficult because the interactions can reduce genetic variation in traits available in the direction of selection (Blows et al. 2004; Blows & Hoffmann 2005).

Gene flow can restrict adaptive responses when there is an influx of alleles from a large source population and these alleles have a low fitness in the environment where climatic selection is occurring. Gene flow can have a particularly large effect in populations adapting to stressful climatic conditions at species borders; if these conditions are not found in other parts of a species range, gene flow into a small border population will limit adaptive responses (Kirkpatrick & Barton 1997). However, the role of gene flow in limiting climatic adaptation has rarely been considered, except in a few local cases (Bridle et al. 2009).

Five types of studies provide data for testing these different hypotheses. Plastic responses can indicate the mechanisms whereby organisms counter climatic variability within their lifetime, such as acclimation that increases resistance to high and low temperatures; these responses might help to identify traits that are constrained in evolution. Detailed studies of genetic polymorphisms can be used to assess antagonistic pleiotropy, by testing whether different alleles are favoured under different conditions. Quantitative genetic approaches including selection experiments can be used to test for antagonistic pleiotropy and whether DNA decay occurs when organisms are confined to one environment. Selection experiments can also be used to assess the ability of populations to respond via changes in multiple traits, although this has rarely been attempted. Species comparisons can be used to test trade-offs associated with ecological specialisation and these might also provide information on DNA decay when the evolutionary history of species is known. Finally, molecular data within a phylogenetic framework can be used to test for patterns of DNA decay in species exposed to different environments; these can then be separated from patterns of selection in candidate genes that might reflect pleiotropic interactions as discussed later.

PLASTIC RESPONSES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES

These responses that alter the fitness of organisms within their lifetime are often interpreted in terms of costs and trade-offs. When conditions that trigger an increase in high temperature resistance have a negative impact on the opposing extreme or optimal performance, this suggests a mechanism that produces a cost and therefore might limit evolutionary adaptation. Costs in plastic responses to climatic conditions are usually interpreted in terms of the ‘beneficial acclimation hypothesis’, where insects exposed to a particular set of conditions have a relatively higher fitness under them than an alternative set of conditions (Huey et al. 1999; Deere & Chown 2006). This pattern has been demonstrated in some species including a parasitoid (Thomson et al. 2001) and a butterfly (Geister & Fischer 2007). However it can be difficult to decide on meaningful conditions for testing the beneficial effects of acclimation. For instance a rearing environment of 25°C might increase fitness under conditions hotter than 25°C, and that are more likely to be encountered by adults reared at 25°C than at a cooler temperature (Gvozdik et al. 2007). For this reason, experiments testing the cost of acclimation should target a range of temperature conditions likely to be experienced in the field at different life cycle stages (Deere & Chown 2006).

For some invertebrates, benefits are difficult to find even across a range of temperatures; this is the case in several oribatid mites (Deere & Chown 2006). However, for many insects both developmental acclimation and short-term exposures to stress can have benefits when countering stressful conditions. For instance, in Drosophila species, rearing acclimation has a large beneficial impact on levels of heat resistance and particularly cold resistance when measured in the laboratory (Hoffmann et al. 2003b). Rearing conditions can have an even larger impact in the field; Drosophila melanogaster Meigen (Diptera, Drosophilidae) adult releases indicate that flies reared under cool conditions are many times more likely to reach food in cold conditions than flies reared under warm conditions (Kristensen et al. 2008).

Given these benefits of thermal acclimation at least under extreme conditions, is there evidence for costs of acclimation mechanisms? Several studies suggest that acclimation can have a negative effect on performance under optimal conditions. For instance, Liriomyza huidobrensis Blanchard (Diptera, Agromyzidae) leafminer adults exposed to mild heat shocks increase heat resistance without influencing cold resistance, but there is also a decrease in fecundity (Huang et al. 2007). Similarly, D. melanogaster with an increased level of heat resistance following acclimation suffer a cost in terms of decreased fecundity under milder conditions (Krebs & Loeschcke 1994). The costs of acclimation under field conditions can be much larger than in the laboratory; heat-hardened D. melanogaster are better at locating field food resources under warm conditions but this comes at a large cost under milder conditions (Loeschcke & Hoffmann 2007), while flies that have developed under cold conditions are up to 36 times less likely to find food than flies reared at an intermediate temperature (Kristensen et al. 2008).

While these findings suggest that plastic responses lead to costs, these might not necessarily translate into evolutionary costs and antagonistic pleiotropy. For evolutionary costs to occur, the mechanisms underlying plastic responses would need to constrain the ability of organisms to evolve under changing climatic conditions. One such mechanism might involve expression of genes producing the heat shock protein HSP70, which is triggered by exposure to stress and represents a plastic response that increases resistance (Krebs & Loeschcke 1994) but may also be associated with an evolutionary cost when too much HSP70 is produced (Sørensen et al. 2001).

SINGLE GENE POLYMORPHISM

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES

These polymorphisms involve alternative allelic forms of the same gene. The genotypes that are formed by the different alleles can provide evidence for a genetic basis to costs/antagonistic pleiotropy. If costs occur, genotypes that perform well under high temperatures (or dry conditions) are expected to perform relatively poorly under optimal conditions or perhaps low temperatures (or wet conditions). Singe gene polymorphisms can thereby provide direct evidence for costs/antagonistic selection at the genetic level.

A few polymorphisms that are involved in the thermal responses of insects have been isolated and suggest antagonistic pleiotropy. The willow beetle Chrysomela aeneicollis Schaeffer (Coleoptera: Chrysomelidae) exhibits genetic polymorphism for the glycolic enzyme phosphoglucose isomerase (PGI) and one allele is common in cooler areas while another is common in warmer areas. These alleles influence the expression of HSP70 (one of the common heat shock proteins in insects) and also influence fecundity, such that the fecundity of genotypes homozygous for alternative alleles is highest under climatic conditions where the alleles are common (Dahlhoff et al. 2008). PGI has also been implicated in dispersal selection in Colias (Lepidoptera: Pieridae) species and other butterflies (Wheat et al. 2006).

Another polymorphism that responds to temperature is the alcohol dehydrogenase gene (Adh) of D. melanogaster. Environmental temperatures alter the frequency of Adh alleles in laboratory and natural populations of D. melanogaster (McKenzie & McKechnie 1983) and there is also evidence that recent climate change has altered clinal patterns in allele frequency along the east coast of Australia (Umina et al. 2005), involving an increase in the allele common in the tropics along the entire cline. Recent data also suggest that climatic selection influences a polymorphism at the isocitrate dehydrogenase locus in the striped ground cricket, Allonemobius socius Scudder (Orthoptera: Trigonidiidae); alleles at this enzyme locus show frequency clines, and the allozymes vary in kinetic parameters with temperature consistent with these clinal patterns and the hypothesis of antagonistic pleiotropy (Huestis et al. 2009). Finally a polymorphism in the structural part of the couch potato gene appears to underlie diapause variation in D. melanogaster (Schmidt et al. 2008). This trait is associated with a raft of life history and stress resistance traits and is likely to have costs and benefits depending on seasonal changes in stressful conditions (Schmidt & Conde 2006).

These examples point to antagonistic pleiotropy as a possible mechanism influencing climatic adaptation, and also suggest that warm climate specialists are likely to have different sets of alleles when compared with cold climate specialists. Although most examples to date involve polymorphisms in the structural part of the gene, regulatory elements also influence adaptive shifts in insect populations (Janssens et al. 2007). Polymorphisms in regulatory elements have been more difficult to study in the past but are now more amenable to genetic and physiological analyses as new genomic tools allow rapid screening for polymorphisms in all parts of the insect's genome.

QUANTITATIVE GENETIC TESTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES

The three hypotheses for climatic specialisation lead to different predictions about patterns of genetic variation in populations. If there is DNA decay in genes underlying traits involved in adaptation to cold or dry conditions, then climate specialists from warm and humid conditions are expected to show little selection response and a low heritability for these traits. Selection responses and heritable variation for traits occurs when there is allelic variation in functional genes and their controlling elements. When genes are decayed and no longer functional, adaptive heritable variation will be low and selection responses become less likely. On the other hand, antagonistic pleiotropy is predicted to produce a selection response that allows a climate specialist to extend its distribution range, but costs will constrain the response. If a complex of traits is responsible for specialisation, there may still be genetic variation in any one trait involved in climatic adaptation, but the different combination of traits required to make an adaptive response might only evolve very slowly when selected together, particularly if there are genetic interactions among the traits.

Antagonistic pleiotropy and costs have been widely considered with respect to insect host specialisation. Although there are cases where costs have been detected when the performance of genotypes from a species is compared across hosts, there is often little evidence for trade-offs that might reflect antagonistic pleiotropy (Futuyma & Moreno 1988). Trade-offs have been less commonly tested in the context of climatic adaptation. Part of the problem is that the fundamental niche of a genotype needs to be fully defined in testing for fitness costs (Palaima 2007) and this is difficult in the context of climatic responses because of plastic responses and differences in the susceptibility of life cycle stages. Thermal trade-offs have been investigated by comparing the performance of strains across different temperatures. Kingsolver et al. (2004) considered growth rates of Pieris rapae L (Lepidoptera: Pieridae) caterpillars across a range of temperatures from 8°C to 40°C and found that growth at 35°C (when it was at a maximum) was negatively correlated genetically with growth at 40°C when there was a sharp decline, suggesting a trade-off between optimal and high temperature performance. Thermal selection experiments in D. melanogaster suggest that heat and cold resistance traits are largely genetically independent but that increased resistance may be accompanied by decreased performance in some life history traits (Mori & Kimura 2008). Selection experiments on desiccation resistance also suggest trade-offs between increased resistance and life history traits that contribute to fitness under non-stressful conditions (Hoffmann & Harshman 1999; Gefen & Gibbs 2009). Thus while increased performance at one extreme is rarely associated with a decrease in performance at the opposite extreme, increased resistance does trade off with performance under non-stressful conditions; these trade-offs probably reflect costs and antagonistic pleiotropy because there is likely to have been insufficient time in most selection experiments for DNA decay and mutation accumulation.

Although selection experiments and strain comparisons might argue against costs between extremes when averaged across loci, it is still possible that particular loci show evidence of antagonistic pleiotropy. These effects can be investigated by considering specific polymorphisms (as discussed above), and also though QTL (quantitative trait locus) mapping experiments where variation in traits is mapped to the effects of specific regions of the genome and then compared across environments. In D. melanogaster, QTL mapping suggests that some genomic regions increasing heat resistance may decrease cold resistance (Norry et al. 2008) although further work is needed to establish if this is due to the same alleles having antagonistic effects or different linked markers (i.e. linkage disequilibrium because of loci affecting different traits being located close together along a chromosome rather than antagonistic pleiotropy).

Although selection experiments suggest that costs can occur between performance at extremes and non-stressful conditions, costs detected within populations and in selection experiments may only last a few generations – they might not necessarily translate into long-term constraints that influence the way traits are correlated across populations and even species. For thermal responses, the best data on costs over a longer time interval come from bacteria where evolution across thousands of generations can be followed experimentally. When 12 experimental populations of the bacterium Escherichia coli evolved for 20 000 generations at 37°C, there was improvement in performance in the range 27–39°C, but decreased growth in most lines at 20°C and 41–42°C (Cooper et al. 2001). Because the loss in fitness mostly occurred at a time when populations were adapting early on, it was thought that pleiotropy was likely to be responsible for the loss of fitness rather than mutation accumulation although this was not directly demonstrated. For E. coli lines evolved for 2000 generations at 20°C, there was a general decline in fitness at 40°C, but not in all lines (Bennett & Lenski 2007). This suggests an overall trade-off in performance consistent with antagonistic pleiotropy, but DNA decay may have contributed to the decrease in performance in some lines. In contrast, loss of sporulation function in experimental populations of Bacillus subtilis developed largely as a consequence of DNA decay rather than selection (Maughan et al. 2007). The loss of function was associated with small insertions and deletions in the DNA or as well as nucleotide substitutions (Maughan et al. 2009).

Data across an equivalent large number of generations are not available for insects, although long-established insect colonies that have been maintained under particular conditions provide an avenue for exploring persistent costs. A field population of the tobacco hornworm, Manduca sexta L (Lepidoptera: Sphingidae), which routinely experiences fluctuating temperatures, performed more poorly under constant thermal conditions than a laboratory population maintained for 250 generations at a constant temperature (Kingsolver et al. 2009). This suggests a possible trade-off associated with adapting to fluctuating conditions. However, the field and laboratory populations performed similarly under diurnal temperature fluctuations, suggesting that laboratory adaptation to constant conditions for 250 generations had occurred without a large cost developing.

If mutations accumulate and genes for adapting to a particular set of environmental conditions become non-functional over time, heritable variation for dealing with those conditions should decrease in the same interval. This leads to the prediction of limited genetic variance in specialist species for traits that are currently limiting their distributions, and a limited response to directional selection on these traits. Although numerous heritability estimates are published in the insect literature each year, there are very few estimates for the same trait measured on a variety of species, particularly for traits that might limit species distributions. In Drosophila birchii Dobzhansky & Mather, a species usually restricted to tropical rainforests, heritable variation for desiccation resistance was investigated with selection experiments (Hoffmann et al. 2003a). This trait shows a rapid response to selection in several species including the cosmopolitan D. melanogaster and D. simulans. However when selection was undertaken on a population of D. birchii, there was no detectable response to selection despite strong selection across many generations (Hoffmann et al. 2003a). Genetic studies involving comparisons among relatives indicate that there is no evidence for heritable variation for desiccation resistance in this species, and also in a second tropical rainforest Drosophila, D. bunnanda Schiffer & McEvey (Kellermann et al. 2006). Thus at least with respect to these species there appears to be a loss of heritable variation for a trait likely to limit species distributions. A more general prediction is that the heritability of a trait determining the distribution of a range of species (like desiccation resistance) is expected to be correlated with the sensitivity of the species. This prediction seems to hold at least in the case of desiccation and cold resistance in Drosophila species for which physiological and phylogenetic data are available (Kellermann et al. 2009).

The only other relevant data for comparing heritable variation across related insect species with different niches is for host plant use in phytophagous insects. In particular, Futuyma et al. (1995) considered larval survival, oviposition and feeding responses of species from the beetle genus Ophraella (Coleoptera: Chrysomelidae) to their congeners' host plants in the Asteraceae. There was no evidence of genetic variation in 18 of 39 tests of feeding responses and 14 of 16 tests of larval survival on congeners' hosts, suggesting that low levels of genetic variation constrain host utilisation in this group. Moreover, heritable variation was restricted to species closely related to the plants used by a particular species, whereas unrelated host species could not be utilised at all. Other studies on host plant use have shown that even when some heritable variation is detected, selection experiments may lead to only a very small response to selection when alternate host plants are tested (Nylin et al. 2005) or else differences among populations can fail to develop when they might be expected to do so (Ballabeni & Rahier 2000; Poore & Steinberg 2001). Host use in related species appears to be constrained even though there are some spectacular documented examples of shifts in host use in populations (Carroll 2007).

Ecological data suggest that climate specialists have consistently narrow niche limits even when there is an opportunity to expand distributions. For instance, biological control agents for weedy species that have a narrow thermal range in their native range also tend to occupy a narrow thermal range after their introduction, even when the host weed is much more widely distributed (Dhileepan et al. 2005). Invertebrate taxa are often limited to a narrow range of conditions and respond in a predictable manner to changes in variables like salinity (Kefford et al. 2005), thermal conditions (Chown 2001) and pollutants like hydrocarbons (Pettigrove & Hoffmann 2005). These restrictions suggest that specialised species are constrained in their evolutionary responses, unlike widespread species that often show a marked range of adaptive responses across their geographic range.

Selection experiments could be used to test the notion that multiple dimensions limit evolutionary responses, but I am unaware of experiments where complex thermal responses across multiple traits have been selected. For host use, strain comparisons in the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), suggest that changes in behavioural and performance traits are uncorrelated, which tends to support the notion that multiple traits evolving independently might make it difficult for host shifts to occur (Forister et al. 2007). For high temperature resistance, selection experiments and strain comparisons with D. melanogaster suggest that different components of heat response are uncorrelated (Hoffmann et al. 2003b), and this might make it more difficult for populations to adapt to increasing temperatures. To function under relatively hotter, drier or colder conditions, insects may need to alter a range of traits associated with mating, resisting thermal extremes and responding behaviourally. However it is still possible that in some cases multiple traits needed for surviving under stressful conditions are controlled by a simple genetic switch, as seems to be the case for the genetic switch controlling diapause in D. melanogaster, which also influences different stress responses and life history traits (Schmidt & Paaby 2008).

SPECIES COMPARISONS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES

In general, insects show a wider range of variation in their lower thermal limits than in their upper thermal limits (Addo-Bediako et al. 2000). Comparisons of thermal limits across insect groups tend to indicate a lack of association between upper and lower thermal limits. For instance, in 10 species and 31 populations of weevils from two Antarctic islands, Klok and Chown (2003) found no evidence of any association between species limits. Data collected across species and populations of Drosophila also suggest no association between high and low thermal limits (Kimura & Beppu 1993; Kimura et al. 1994).

Nevertheless some mechanisms of thermal and aridity responses might lead to antagonistic pleiotropy at the interspecific level. For instance, melanism tends to be higher in ectotherms from cool environments (Clusella Trullas et al. 2007), assisting species in achieving higher body temperatures for activity. Insects with a high level of melanism might also benefit from a decrease in the rate of water loss, leading to an increase in desiccation resistance (Parkash et al. 2008). Under hot conditions melanism is likely to be a disadvantage for species because dark individuals tend to warm up relatively more quickly and then become heat stressed.

Except where information is available on specific mechanisms, it is usually difficult in species comparisons to separate the contributions made to trade-offs by antagonistic pleiotropy and DNA decay. Unless there is a history of hybridisation among species, they have usually undergone a long history of independent evolution. Within this selection history, differences in environmental performance may have developed because of the fixation of alleles demonstrating antagonistic pleiotropy, or because of the accumulation of mutations. Perhaps the only way of separating these hypotheses – short of testing and demonstrating decay or selection in candidate genes – is to have an intimate knowledge of the evolutionary history of a group. A loss of performance in an environment might occur too quickly to be accounted for by decay, or it might match a period when selection was occurring and pleiotropic effects were therefore expected to lead to trade-offs. Perhaps species might show little loss of performance in an environment despite a long history of being restricted to a different environment, in which case hypotheses other than pleiotropy and decay might contribute to specialisation.

Where ancestral characteristics within phylogenies are available, it may be possible to reconstruct the history of evolutionary changes leading to climatic adaptation and specialisation. Goto et al. (2000) analysed phylogenetic relationships and levels of low and high temperature resistance in Drosophila species from the montium and takahashii species groups. They suggested that temperate species in these groups evolved from subtropical highland species, because these highland species showed retarded ovarian development at a low temperature, a feature also possessed by the temperate species and likely to assist in overwintering at the adult stage. The highland species may have been pre-adapted to temperate areas, unlike tropical lowland species. However the highland group had a lower level of cold resistance than the temperate species, suggesting that this character evolved within the temperate species, and with little loss of heat resistance, which tended to be higher in the temperate group when compared with the highland species. These findings reinforce the notion that trade-offs are probably not closely associated with adaptation to thermal extremes.

When the evolutionary relationship among species is known it is possible to test for phylogenetic constraints. There is evidence for phylogenetic constraints on climatic adaptation in some groups but not in others. Psyllids show only limited phylogenetic signal for the climatic conditions they occupy (Hodkinson 2009); temperate and tropical species occur in many groups, and the potential for adaptation to different climate regions appears to persist at least over millions of years. In contrast, there seems to be a strong phylogenetic signal in Drosophila for traits involved in stress resistance (e.g. Matzkin et al. 2009). In the wasp genus Coccygomimus (Hymenoptera: Ichneumonidae) diapause responses are constrained by phylogeny rather than geographic distribution (Yasuhara et al. 1998). Calliphora (Diptera: Calliphoridae) blowflies that originated in the cool Holarctic also seem to be constrained because a member of this genus from a warm environment has reduced upper thermal thresholds at all life cycle stages when compared with other blowflies inhabiting the same area but with ancestors from warmer environments (Richards et al. 2009).

Phylogenetic constraints could reflect DNA decay if this process is difficult to reverse through evolutionary processes like gene duplication. Related species might then become restricted to particular climatic conditions, although this assumes that species from different branches of a phylogeny have had the opportunity to adapt to different climates. Conversely, if function is maintained despite species being exposed to different environments, DNA decay might not be effective. With respect to host plant use, Scriber et al. (2008) found that species of Papilionidae (Lepidoptera) from North America and Australia tested on Australian host plant families were still capable of using a wider range of hosts from different families of plants than they normally used, suggesting the persistence of ancient detoxification mechanisms over millions of years. In this case DNA decay may not have affected the function of the detoxification genes although these genes may also have maintained functionality because of pleiotropic effects, such as through a role in insect hormone synthesis (Chung et al. 2009).

GENETIC SIGNATURES OF SPECIALISATION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES

Decay and pleiotropy leave different signatures of selection in genes at the DNA level. If selection acts to favour a particular allele that sweeps through a population, there is a decrease in genetic variation generally around the allele that is selected (i.e. linked closely to the allele on the same chromosome). A particular nucleotide difference or insertion/deletion (indel) in the DNA that distinguishes the allele will be at linkage disequilibrium with other polymorphisms nearby. Therefore when a new favoured allele arises and spreads it will also cause other changes, effectively sweeping away nearby DNA variation. These changes will disappear over time because of ongoing mutation and recombination restoring genetic variation in the adjacent region.

Such signatures have been detected in insect genes known to be under selection. In D. melanogaster, insecticide resistance genes show patterns of reduced genetic variation around alleles under selection, suggesting past selective sweeps (Catania et al. 2004). Sweeps have also been detected for genes involved in olfactory and gustatory responses both in Drosophila and in aphids (McBride 2007; Smadja et al. 2009). In the pea aphid, several of the olfactory and gustatory receptor genes not found in other insects show evidence of positive selection reflecting recent evolutionary divergence (Smadja et al. 2009). Few climate genes have so far been examined from this perspective, although in Drosophila selection on regulatory sequences leading to changes in body pigmentation has recently been elucidated (e.g. Jeong et al. 2008) and patterns of gene conversion in heat shock genes have been interpreted in terms of selective sweeps (Bettencourt & Feder 2002).

DNA decay is not expected to generate any decrease in variation around sites under selection. Instead, there will be a gradual decay in a gene as it evolves towards becoming a non-functional pseudogene. Models of pseudogene evolution assume that mutational changes in pseudogenes occur as if they are neutral (Fleishman et al. 2003). Pseudogenes therefore are subject to different nucleotide substitution patterns than functional genes: the latter have different substitution rates at the first, second and third codon position whereas pseudogenes are expected to have the same rate of nucleotide substitution at all positions. If the pseudogene is an orthologue, its evolution could follow neutrality as soon as it is duplicated. If the pseudogene is a paralogue, it may become non-functional rapidly or gradually depending on whether there are any remaining selective constraints acting on the gene. The time to inactivation depends on the nature of mutations accumulating in the pseudogene. It could be extremely rapid if only a single mutation leading to a stop codon arises and spreads (and assuming that the resulting protein becomes non-functional because it is truncated too far).

As the process of DNA decay progresses, there will be differences in the number of pseudogenes carried in closely related species. This is particularly evident in microorganisms. For instance, the causative agent of leprosy, Mycobacterium leprae, has a large estimated number (>1000) of pseudogenes compared with its relative Mycobacterium tuberculosis, which has only six (Babu 2003). This difference may be associated with the presence of sigma factors, a class of proteins that determine specificity of RNA polymerase, and thereby regulates groups of genes. In M. leprae several sigma factors have become pseudogenes; this in turn could have triggered the development of other pseudogenes because groups of genes influenced by these sigma factors were no longer triggered by functional sigma factors under specific sets of conditions.

In insects, loss of function has been detected in genes that are involved in sensing an environment. In subterranean diving beetles, Leys et al. (2005) characterised changes in the eye colour gene cinnabar. Eyeless lineages have an increased rate of sequence evolution and the presence of mutations leading to frameshifts and stop codons when compared with eyed species. The proportion of non-synonymous to synonymous substitutions was also relatively higher in the eyeless species. The cinnabar gene was therefore behaving like a pseudogene in these lineages.

There is evidence of DNA decay and gene loss in Drosophila species that have undergone ecological shifts. Drosophila sechellia Tsacas & Bachli, a specialist species, reproduces on the ripe fruit of Morinda citrifolia, which is toxic to related species. This species is confined to the Seychelles and is closely related to the cosmopolitan species D. melanogaster. Host specialisation in this case has involved the loss of genes for recognising odours from the normally toxic fruit as well as loss of some bitter taste receptor genes (McBride 2007; Matsuo 2008). The loss of the odour recognition genes is likely to be a direct adaptive response, but changes in the bitter tasting genes might reflect a DNA decay process. In general, patterns of divergence in odorant-binding protein (OBP) families in Drosophila fit a ‘birth and death’ model; there have been 43 gene gains and 28 gene losses, the latter consisting of 15 deletions and 13 pseudogenisation events (Vieira et al. 2007). This can lead to related species having quite different sets of chemoreception genes (Smadja et al. 2009).

In microorganisms, the types of active genes present in a genome can be used to infer the nature of the environment occupied by the organism and vice versa (Pal et al. 2006). This is not yet possible in insects, although it has been speculated that the presence/absence of particular families of genes might reflect ancestral environments. For instance, the absence of detoxification genes in the honey bee genome is likely to reflect low levels of toxins in the environment occupied by honey bees (Consortium 2006). The presence of particular families of genes like heat shock proteins might eventually be related to climate responses. However genes involved in climate responses might instead tend to be involved in multiple functions that include essential processes. For instance, many heat shock protein genes are expressed at low levels during development where they have essential functions (e.g. Timakov & Zhang 2001). In that case, the composition of gene families might not be altered much due to climatic selection. Instead subtle changes in expression levels, tissue distribution of expression and gene products and/or temporal patterns of expression might then influence climatic adaptation.

WHICH PROCESS IS MORE IMPORTANT?

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES

The relative importance of antagonistic pleiotropy vs. DNA decay and other processes in driving specialisation has only really been assessed in digital organisms and in bacteria. In simulations on digital organisms (Ostrowski et al. 2007), the organisms gain energy from computations with numbers obtained from the environment. Specialisation is modelled by allowing energy from only one type of computation. When these organisms are allowed to evolve, the loss of ability to perform other computations is driven by neutral and deleterious mutations, highlighting the potential importance of decay, although antagonistic pleiotropic mutations also contributed to specialisation. As mentioned above, E. coli adapting for 20 000 generations to 37°C tend to show decreased growth to both higher and lower extremes; these patterns appear to be due to antagonistic pleiotropy rather than DNA decay (Cooper et al. 2001). However in other studies on specialisation in microorganisms, DNA decay often also appears to play an important role (Maughan et al. 2007; Presloid et al. 2008).

In insects and particularly in Drosophila, there is ample evidence that increased resistance to thermal extremes and aridity has costs, particularly in terms of optimal performance. Antagonistic pleiotropy therefore emerges as an important component of climatic specialisation and some polymorphisms that act in this manner have been identified in several insect species. The contribution of DNA decay to climate specialisation has been explored to a lesser extent but comparative genomic studies highlight the dynamic nature of insect genomes, and there is potential to eventually link gene loss and gain as well as loss of function to environmental conditions. Comparative studies on candidate sets of genes underlying climate adaptation and comparative studies on genetic variance in traits associated with climate adaptation and trait interactions should provide an opportunity to further test the importance of pleiotropy and decay. The involvement of trait multidimensionality and gene flow in limiting climatic adaptation has rarely been explored but deserves further investigation, particularly as a number of mechanisms can contribute to climatic adaptation. These include changes in timing of reproduction, behavioural responses to temperature and humidity, plastic responses, morphological changes and the ability to tolerate extremes. Given the number and impact of evolutionary processes leading to climatic and host specialisation, it is perhaps not surprising that the majority of insects are specialists.

ACKNOWLEDGEMENTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES

I am grateful to Roger Kitching and Jane Hughes for comments on an earlier version of this paper. My research on evolutionary responses in insects to climate change is supported by the Australian Research Council and the Commonwealth Environmental Research Fund.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PLEIOTROPY, LOSS OF GENE FUNCTION AND MULTIDIMENSIONALITY
  5. PLASTIC RESPONSES
  6. SINGLE GENE POLYMORPHISM
  7. QUANTITATIVE GENETIC TESTS
  8. SPECIES COMPARISONS
  9. GENETIC SIGNATURES OF SPECIALISATION
  10. WHICH PROCESS IS MORE IMPORTANT?
  11. ACKNOWLEDGEMENTS
  12. REFERENCES