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Male-specific genotype by environment interactions influence viability selection acting on a sexually selected inversion system in the seaweed fly, Coelopa frigida
Abstract
In the seaweed fly, Coelopa frigida, a large chromosomal inversion system is affected by sexual selection and viability selection. However, our understanding of the interaction between these two selective forces is currently limited as research has focused upon a limited range of environments. We allowed C. frigida larvae to develop in two different algae, Fucus and Laminaria, and then measured viability and body size for each inversion genotype. Significant male-specific genotype-by-environment interactions influenced viability and body size. For males developing in Laminaria, the direction of viability selection acts similarly on the inversion system as the direction of sexual selection. In contrast, for males developing in Fucus, viability selection opposes sexual selection. These results demonstrate that through considering viability selection in different environments, the costs and benefits associated with sexual selection can be found to vary.
... The DNA marker consisted of two single-nucleotide polymorphisms that were associated with the different inversion rearrangements, and these were genotyped with two restriction enzymes (detailed in electronic supplementary material, table S1 and figure S1). It was validated with 44 samples previously karyotyped with the allozyme procedure as described by Edward et al. [34] (electronic supplementary material, table S2) and subsequently used to characterize the karyotype of 1988 wild American samples of C. frigida (89 -117 individuals/population; electronic supplementary material, table S4). For each population, the frequency of a rearrangement and the proportion of each karyotype were calculated in males and females separately, and then estimated for both sexes pooled at a sex-ratio of 1 : 1. ...
... Our data suggest that the relative proportions of seaweed species vary with habitat on which each karyotype is preferentially adapted. Both in Europe and America, an increased abundance of Laminariaceae is associated with an increased proportion of aa karyotypes (electronic supplementary material, figure S9), a result which is consistent with better survival of aa on Laminariaceae in the laboratory [34]. Mixed wrackbeds or plant debris favours heterokaryotypes while wrackbeds of Fucaceae or other seaweeds are associated with increased proportions of bb. ...
... The amount of resources available in each substrate may be one of the factors explaining the different karyotype proportions. In fact, in the laboratory, Laminariaceae sustain a greater viability and a larger size than Fucaceae [34], which suggests it is a richer substrate, facilitating the long larval development and the large size of aa. In the wild populations investigated here, higher aa proportions are also found in populations with large flies (all karyotypes/sexes), and insect size is generally a good indicator of larval growth conditions [68]. ...
Large chromosomal rearrangements are thought to facilitate adaptation to heterogeneous environments by limiting genomic recombination. Indeed, inversions have been implicated in adaptation along environmental clines and in ecotype specialization. Here, we combine classical ecological studies and population genetics to investigate an inversion polymorphism previously documented in Europe among natural populations of the seaweed fly Coelopa frigida along a latitudinal cline in North America. We test if the inversion is present in North America and polymorphic, assess which environmental conditions modulate the inversion karyotype frequencies, and document the relationship between inversion karyotype and adult size. We sampled nearly 2000 flies from 20 populations along several environmental gradients to quantify associations of inversion frequencies to heterogeneous environmental variables. Genotyping and phenotyping showed a widespread and conserved inversion polymorphism between Europe and America. Variation in inversion frequency was significantly associated with environmental factors, with parallel patterns between continents, indicating that the inversion may play a role in local adaptation. The three karyotypes of the inversion are differently favoured across micro-habitats and represent life-history strategies likely to be maintained by the collective action of several mechanisms of balancing selection. Our study adds to the mounting evidence that inversions are facilitators of adaptation and enhance within-species diversity.
... Although those factors may correlate with the duration of the wrackbed stability, they are also known to modulate the genotype-phenotype relationships and therefore the associated fitness. Controlled experiments in C. frigida show that substrate composition, temperature and density affect the relationship between genotype and survival, development time, body weight and body size (G × E effect) 33,38,51,52 . In nature, this translates to geographic variation in male and female sizes, as well as variation in size difference among genotypes and between the sexes 26,36 . ...
... C. frigida provides an empirical case of antagonistic pleiotropy whereby the strength of selection, but not the direction, differs between sexes for each fitness component. Differences between genotypes in size, development time, fertility and survival are stronger for males than for females 33,35,36,52 . Within a range of realistic parameters, sex-specific effects, even without antagonism for each fitness components, results in sexual antagonism for total fitness, therefore strongly protecting polymorphism 19 . ...
How natural diversity is maintained is an evolutionary puzzle. Genetic variation can be eroded by drift and directional selection but some polymorphisms persist for long time periods, implicating a role for balancing selection. Here, we investigate the maintenance of a chromosomal inversion polymorphism in the seaweed fly Coelopa frigida. Using experimental evolution and quantifying fitness, we show that the inversion underlies a life-history trade-off, whereby each haplotype has opposing effects on larval survival and adult reproduction. Numerical simulations confirm that such antagonistic pleiotropy can maintain polymorphism. Our results also highlight the importance of sex-specific effects, dominance and environmental heterogeneity, whose interaction enhances the maintenance of polymorphism through antagonistic pleiotropy. Overall, our findings directly demonstrate how overdominance and sexual antagonism can emerge from a life-history trade-off, inviting reconsideration of antagonistic pleiotropy as a key part of multi-headed balancing selection processes that enable the persistence of genetic variation.
... The flies experience high mortality during the early larval phase (Butlin & Day, 1984;Cullen et al., 1987), with mortality and growth rates differing based on the seaweed composition within the wrackbed (Cullen et al., 1987;Edward, 2008). As bacterial assemblages likely shift with seaweed composition, this suggests that the wrackbed microbiome could exert significant selective pressure on C. frigida (Edward, 2008;Edward & Gilburn, 2013), pointing towards a potential importance of the wrackbed microbiome for higher trophic levels. However, whether or not the wrackbed microbiome is a driver of selection in this species remains unknown. ...
Sandy beaches are biogeochemical hotspots that bridge marine and terrestrial ecosystems via the transfer of organic matter, such as seaweed (termed wrack). A keystone of this unique ecosystem is the microbial community, which helps to degrade wrack and re-mineralize nutrients. However, little is known about this community. Here, we characterize the wrackbed microbiome as well as the microbiome of a primary consumer, the seaweed fly Coelopa frigida, and examine how they change along one of the most studied ecological gradients in the world, the transition from the marine North Sea to the brackish Baltic Sea. We found that polysaccharide degraders dominated both microbiomes, but there were still consistent differences between wrackbed and fly samples. Furthermore, we observed a shift in both microbial communities and functionality between the North and Baltic Sea driven by changes in the frequency of different groups of known polysaccharide degraders. We hypothesize that microbes were selected for their abilities to degrade different polysaccharides corresponding to a shift in polysaccharide content in the different seaweed communities. Our results reveal the complexities of both the wrackbed microbial community, with different groups specialized to different roles, and the cascading trophic consequences of shifts in the near shore algal community.
... 4 the Cf-Inv(1) chromosomal inversion (Day, Dawe et al. 1983, Butlin and Day 117 1989, Wellenreuther, Rosenquist et al. 2017, Berdan, Rosenquist et al. 2018, 118 Mérot, Berdan et al. 2018). This suggests that the wrackbed microbiome could 119 exert significant selective pressure on both C. frigida and even on the Cf-Inv(1) 120 inversion itself (Edward 2008, Edward andGilburn 2013), pointing towards a 121 potential importance of the wrackbed microbiome for higher trophic levels. 122 ...
23 24 Sandy beaches are biogeochemical hotspots that bridge marine and terrestrial 25 ecosystems via the transfer of marine organic matter, such as seaweed (termed 26 wrack). A keystone of this unique ecosystem is the microbial community, which 27 helps to degrade wrack and re-mineralize nutrients. However, little is known 28 about the wrackbed microbiome, its composition, trophic ecology, or how it 29 varies over time and space. Here we characterize the wrackbed microbiome as 30 well as the microbiome of a primary consumer, the seaweed fly Coelopa frigida, 31 and examine how they change along one of the most studied ecological gradients 32 in the world, the transition from the marine North Sea to the brackish Baltic Sea. 33 We found that polysaccharide degraders dominated both the wrackbed and 34 seaweed fly microbiomes but there were still consistent differences between 35 wrackbed and fly samples. Furthermore, we observed a shift in both microbial 36 communities and functionality between the North and Baltic Sea. These shifts 37 were mostly due to changes in the frequency of different groups of known 38 polysaccharide degraders (Proteobacteria and Bacteroidota). We hypothesize 39 that microbes were selected for their abilities to degrade different 40 polysaccharides corresponding to a shift in polysaccharide content in the 41 seaweed communities of the North vs. Baltic Sea. Our results reveal the 42 complexities of both the wracked microbial community, with different groups 43 specialized to different roles, and the cascading trophic consequences of shifts in 44 the near shore algal community. 45 46
... The largest of these inversions is Cf-Inv(1), encapsulates 10% of the genome and has two arrangements: α and β. These alternative Cf-Inv(1) arrangements have opposing effects on body size, fertility and development time, a combination of traits which results in different fitness depending on the local characteristics of the wrackbed (Butlin, Read, et al. 1982;Day et al. 1983;Butlin and Day 1985;Edward and Gilburn 2013;Wellenreuther et al. 2017;Berdan et al. 2018;Mérot et al. 2018;Mérot, Llaurens, et al. 2020). Almost nothing is known about the other inversions but, given that a large fraction of the C. frigida genome is impacted by polymorphic inversions, one can expect that these rearrangements play a significant role in structuring genetic variation and in enabling local adaptation. ...
Across a species range, spatially-varying environments can drive the evolution of local adaptation. Multiples sources of environmental heterogeneity, at small and large scales, draw complex landscapes of selection which may challenge adaptation, particularly when gene flow is high. Because linkage opposes gene flow but also limits the efficiency of natural selection by contrasting pressures, the key to multidimensional adaptation may reside in the heterogeneity of recombination along the genome. Structural variants like chromosomal inversions are important recombination modifiers that form massive co-segregating genomic blocks linking together alleles at numerous genes. In this study, we investigate the influence of chromosomal rearrangements on genetic variation to ask how their contribution to adaptation with gene flow varies across geographic scales. We sampled the seaweed fly Coelopa frigida along a bioclimatic gradient of 10° of latitude, a salinity gradient and across a range of heterogeneous, patchy habitats. We assembled a high-quality genome to analyse 1,446 low-coverage whole-genome sequences, and we found large non-recombining genomic regions, including putative inversions. In contrast to the collinear regions depicting extensive gene flow, inversions and low-recombining regions differentiated populations more strongly, either along an ecogeographic cline or at a fine-grained scale. Those genomic regions were disproportionately involved in associations with environmental factors and adaptive phenotypes, albeit with contrasting patterns between the different recombination modifiers. Altogether, our results highlight the importance of recombination in shaping the selection-migration balance and show that a set of several inversions behave as modular cassettes facilitating adaptation to environmental heterogeneity at local and large scales.
... Although those factors may correlate with the duration of the wrackbed stability, they are also known to modulate the genotype-phenotype relationships and therefore the associated fitness. Controlled experiments in C. frigida show that substrate composition, temperature and density affect the relationship between genotype and survival, development time, body weight and body size (GxE effect) (37,41,55,56). In nature, this translates into geographic variation in adult size differences among genotypes and between the sexes (30,40), which may modify the reproductive advantage associated with the α allele. ...
How genetic diversity is maintained in natural populations is an evolutionary puzzle. Over time, genetic variation within species can be eroded by drift and directional selection, leading to the fixation or elimination of alleles. However, some loci show persistent variants at intermediate frequencies for long evolutionary time-scales, implicating a role of balancing selection, but studies are seldom set up to uncover the underlying processes. Here, we identify and quantify the selective pressures involved in the widespread maintenance of an inversion polymorphism in the seaweed fly Coelopa frigida , using an experimental evolution approach to estimate fitness associated with different allelic combinations. By precisely evaluating reproductive success and survival rates separately, we show that the maintenance of the polymorphism is governed by a life-history trade-off, whereby each inverted haplotype has opposed pleiotropic effects on survival and reproduction. Using numerical simulations, we confirm that this uncovered antagonism between natural and sexual selection can maintain inversion variation in natural populations of C. frigida . Moreover, our experimental data highlights that inversion-associated fitness is affected differently by sex, dominance and environmental heterogeneity. The interaction between these factors promotes polymorphism maintenance through antagonistic pleiotropy. Taken together, our findings indicate that combinations of natural and sexual selective mechanisms enable the persistence of diverse trait in nature. The joint dynamics of life history trade-offs and antagonistic pleiotropy documented here is likely to apply to other species where large phenotypic variation is controlled by structural variants.
Significance statement
Persistence of chromosomal rearrangements is widespread in nature and often associated with divergent life-history traits. Understanding how contrasted life-history strategies are maintained in wild populations has implications for food production, health and biodiversity in a changing environment. Using the seaweed fly Coelopa frigida, we show that a polymorphic chromosomal inversion is maintained by a trade-off between survival and reproduction, and thus provide empirical support for a role of balancing selection via antagonistic pleiotropy. This mechanism has long been overlooked because it was thought to only apply to a narrow range of ecological scenarios. These findings empirically reinforce the recent theoretical predictions that co-interacting factors (dominance, environment and sex) can lead to polymorphism maintenance by antagonistic pleiotropy and favour life-history variation.
Coelopidae (Diptera), known as kelp flies, exhibit an ecological association with beached kelp and other rotting seaweeds. This unique trophic specialization necessitates significant adaptations to overcome the limitations of an algal diet. We aimed to investigate whether the flies’ microbiome could be one of these adaptive mechanisms. Our analysis focused on assessing composition and diversity of adult and larval microbiota of the kelp fly Coelopa frigida. Feeding habits of the larvae of this species have been subject of numerous studies, with debates whether they directly consume kelp or primarily feed on associated bacteria. By using a 16S rRNA metabarcoding approach, we found that the larval microbiota displayed considerably less diversity than adults, heavily dominated by only four operational taxonomic units (OTUs). Phylogenetic placement recovered the most dominant OTU of the larval microbiome, which is the source of more than half of all metabarcoding sequence reads, as an undescribed genus of Orbaceae (Gammaproteobacteria). Interestingly, this OTU is barely found among the 15 most abundant taxa of the adult microbiome, where it is responsible for less than 2% of the metabarcoding sequence reads. The other three OTUs dominating the larval microbiome have been assigned as Psychrobacter (Gammaproteobacteria), Wohlfahrtiimonas (Gammaproteobacteria), and Cetobacterium (Fusobacteriota). Moreover, we also uncovered a distinct shift in the functional composition between the larval and adult stages, where our taxonomic profiling suggests a significant decrease in functional diversity in larval samples. Our study offers insights into the microbiome dynamics and functional composition of Coelopa frigida.
Across a species range, multiple sources of environmental heterogeneity, at both small and large scales, create complex landscapes of selection, which may challenge adaptation, particularly when gene flow is high. One key to multidimensional adaptation may reside in the heterogeneity of recombination along the genome. Structural variants, like chromosomal inversions, reduce recombination, increasing linkage disequilibrium among loci at a potentially massive scale. In this study, we examined how chromosomal inversions shape genetic variation across a species range, and ask how their contribution to adaptation in the face of gene flow varies across geographic scales. We sampled the seaweed fly Coelopa frigida along a bioclimatic gradient stretching across 10° of latitude, a salinity gradient and a range of heterogeneous, patchy habitats. We generated a chromosome-level genome assembly to analyse 1,446 low-coverage whole genomes collected along those gradients. We found several large non-recombining genomic regions, including putative inversions. In contrast to the collinear regions, inversions and low recombining regions differentiated populations more strongly, either along an ecogeographic cline or at a fine-grained scale. These genomic regions were associated with environmental factors and adaptive phenotypes, albeit with contrasting patterns. Altogether, our results highlight the importance of recombination in shaping adaptation to environmental heterogeneity at local and large scales.
Understanding how environmental variation drives phenotypic diversification within species is a major objective in evolutionary biology. The seaweed fly Coelopa frigida provides an excellent model for the study of genetically driven phenotypes because it carries an α/β inversion polymorphism that affects body size. Coelopa frigida inhabits highly variable beds of decomposing seaweed on the coast in Scandinavia thus providing a suitable test ground to investigate the genetic effects of substrate on both the frequency of the inversion (directional selection) and on the phenotype (genotype × environment effects). Here we use a reciprocal transplant experiment to test the effect of the α/β inversion on body size traits and development time across four suitable natural breeding substrates from the clinal distribution. We show that while development time is unaffected by G × E effects, both the frequency of the inversion and the relative phenotypic effects of the inversion on body size differ between population × substrate combinations. This indicates that the environment modulates the fitness as well as the phenotypic effects of the inversion karyotypes. It further suggests that the inversion may have accumulated qualitatively different mutations in different populations that interact with the environment. Together our results are consistent with the idea that the inversion in C. frigida likely evolves via a combination of local mutation, G × E effects, and differential fitness of inversion karyotypes in heterogeneous environments.
This chapter examines the consequences of genotype-by-social environment interactions (GSEIs) for the evolution of male sexual traits and, more generally, the operation of sexual selection. It starts by developing a series of simple quantitative genetic models to illustrate the importance of GSEIs to the evolutionary process and how they differ from standard GEIs when the environment is abiotic and therefore does not contain genes. The chapter provides a brief overview of how to measure GSEIs, as well as a discussion of empirical studies that have quantified GSEIs in the context of sexual selection. It concludes by suggesting some fruitful avenues for future research that will stimulate more studies to examine the importance of GSEIs in sexual selection.
Sexual selection has resulted in some of the most captivating features of insects, including flashy colors, bizarre structures, and complex pheromones. These features evolve in dynamic environments, where conditions can change rapidly over space and time. However, only recently has ecological complexity been embraced by theory and practice in sexual selection. We review replicated selection studies as well as studies on variation in the agents of selection to delineate gaps in current knowledge and clarify exciting new directions for research. Existing work suggests that fluctuations in sexual selection may be extremely common, though work on the ecological factors influencing these fluctuations is scarce. We suggest that deeper ecological perspectives on sexual selection may alter some of the fundamental assumptions of sexual selection theory and rapidly lead to new discoveries. Expected final online publication date for the Annual Review of Entomology Volume 59 is January 07, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
An association is reported between the / inversion polymorphism on chromosome I and adult size as assessed by the length of wings, flies are larger than flies, with heterokaryotypes intermediate, and the differences are more marked in males than in females. Laboratory mating experiments were performed in which a single female was given a choice of two males. By examining the genotypes of the progeny larvae, it is shown that the larger male is successful in a significantly greater proportion of trials than the smaller one. This mating success is dependent on the size difference between the males and on the female size. Together these observations suggest an indirect influence of the inversion on male mating success. The possible relevance of this effect to the maintenance of the inversion polymorphism in natural populations is discussed.
Female lesser wax moths (Achroia grisella) choose males based on characters of their ultrasonic advertisement signals. Because a female's opportunity to obtain increased somatic benefits by mating with a particular male is limited, we investigated whether females obtain genetic benefits for their offspring via mate choice. Controlled breeding experiments conducted under favourable food and temperature conditions showed that developmental characters are heritable, that sire attractiveness and offspring survivorship are unrelated, but that females mating with attractive signallers produce offspring who mature faster than the offspring of females mating with non-attractive signallers. However, under some unfavourable food or temperature conditions, it is the offspring of females mating with non-attractive males who mature faster; these offspring are heavier as well. Thus, the relationship between male attractiveness and offspring development is not environmentally robust, and support for a good genes model of mate choice in A. grisella is dependent on conditions. These findings suggest genotype-environment interactions and emphasize the necessity of testing sexual selection models under a range of natural environments.
Several theoretical studies have shown that niche breadth evolution is weighted by gene flow and selection pressures to maintain adaptation within the current niche. However, these studies have assumed that mating pairs form at random within demes. I extend previous models to include sexual selection and find that non-random mating can alter the likelihood of niche expansion in mainland/island structured populations. Under random mating, an allele that improves fitness on the island will only spread if individuals are more than compensated in island fitness for any loss of mainland fitness. In contrast, under sexual selection, an island-adapted allele can spread even when it causes a complete loss of fitness on the mainland.
Sexual selection is responsible for much of the spectacular natural diversity of mating traits. It is unclear, however, how this powerful evolutionary force affects the evolution of traits unrelated to mating. Four recent theoretical studies have argued that sexual selection might increase the rate of adaptation, but each relies on the assumption of a substantial positive covariance between male condition (non-mating fitness) and display. Here we demonstrate, with an explicit genetic model, that sexual selection itself can easily lead to the evolution and maintenance of this covariance. This process occurs through the evolution of condition-dependent male display and the resultant transfer of genetic variance for condition into variance in male display. We also track the effect of the covariance between condition and display on the rate of adaptation. Our results demonstrate a powerful synergy between natural and sexual selection that can elevate population mean fitness. Moreover, this synergy can greatly accelerate the rate of adaptation, making the feedback between natural and sexual selection a particularly potent force in changing environments. This has important implications for several key evolutionary processes, including the evolution of sex, sexual conflict and speciation.
Fitting generalised linear models (GLMs) with more than one predictor has become the standard method of analysis in evolutionary and behavioural research. Often, GLMs are used for exploratory data analysis, where one starts with a complex full model including interaction terms and then simplifies by removing non-significant terms. While this approach can be useful, it is problematic if significant effects are interpreted as if they arose from a single a priori hypothesis test. This is because model selection involves cryptic multiple hypothesis testing, a fact that has only rarely been acknowledged or quantified. We show that the probability of finding at least one 'significant' effect is high, even if all null hypotheses are true (e.g. 40% when starting with four predictors and their two-way interactions). This probability is close to theoretical expectations when the sample size (N) is large relative to the number of predictors including interactions (k). In contrast, type I error rates strongly exceed even those expectations when model simplification is applied to models that are over-fitted before simplification (low N/k ratio). The increase in false-positive results arises primarily from an overestimation of effect sizes among significant predictors, leading to upward-biased effect sizes that often cannot be reproduced in follow-up studies ('the winner's curse'). Despite having their own problems, full model tests and P value adjustments can be used as a guide to how frequently type I errors arise by sampling variation alone. We favour the presentation of full models, since they best reflect the range of predictors investigated and ensure a balanced representation also of non-significant results.
Ecological speciation is considered an adaptive response to selection for local adaptation. However, besides suitable ecological
conditions, the process requires assortative mating to protect the nascent species from homogenization by gene flow. By means
of a simple model, we demonstrate that disruptive ecological selection favors the evolution of sexual preferences for ornaments
that signal local adaptation. Such preferences induce assortative mating with respect to ecological characters and enhance
the strength of disruptive selection. Natural and sexual selection thus work in concert to achieve local adaptation and reproductive
isolation, even in the presence of substantial gene flow. The resulting speciation process ensues without the divergence of
mating preferences, avoiding problems that have plagued previous models of speciation by sexual selection.
Exaggerated sexual displays are often supposed to indicate the indirect benefits females may receive from sexual reproduction with displaying males, but empirical evidence for positive relationships between the genetic quality and sexual trait quality is scant. The explanation for this might lie in the fact that mixing of reproductive individuals whose development has been influenced by genotype-by-environment interactions (GEIs) can blur the relationship between the individual male genetic quality and phenotype as perceived by females. Strong GEIs can generate an ecological crossover, where different genotypes are superior in environments that are separated either in space or time. Here, we use a stochastic simulation model to show that even a weak GEI, which does not generate an obvious ecological crossover, can neutralize or even reverse the relationship between genetic quality and sexual trait size in the presence of environmental heterogeneity during development. Our model highlights the importance of developmental selection in evolution of traits and allows us to predict the situations in which sexual displays might not be reliable indicators of genetic quality.
Samples of the seaweed fly, Coelopa frigida, from six populations widely spaced around the English coast were collected during 1974-76 and again in 1979-80. Gene frequencies at the Alcohol dehydrogenase (Adh) locus were found not to vary significantly between sites, nor over the five year period of their study. Genotype distributions are compared with Hardy-Weinberg expectations and show consistent, mostly significant, differences. These results are interpreted in the light of an association between the Adh locus and a chromosomal inversion polymorphism. It is argued that the remarkable geographical uniformity must indicate the presence of strong selection, probably taking the form of heterokaryotypic advantage.
A guide to using S environments to perform statistical analyses providing both an introduction to the use of S and a course in modern statistical methods. The emphasis is on presenting practical problems and full analyses of real data sets.
The net effect of sexual selection on nonsexual fitness is controversial. On one side, elaborate display traits and preferences for them can be costly, reducing the nonsexual fitness of individuals possessing them, as well as their offspring, In contrast, sexual selection may reinforce nonsexual fitness if an individual's attractiveness and quality are genetically correlated. According to recent models, such good-genes mate choice should increase both the extent and rate of adaptation. We evolved 12 replicate populations of Drosophila serrata in a powerful two-way factorial experimental design to test the separate and combined contributions of natural and sexual selection to adaptation to a novel larval food resource. Populations evolving in the presence of natural selection had significantly higher mean nonsexual fitness when measured over three generations (13-15) during the course of experimental evolution (16-23% increase). The effect of natural selection was even more substantial when measured in a standardized, monogamous mating environment at the end of the experiment (generation 16; 52% increase). In contrast, and despite strong sexual selection on display traits, there was no evidence from any of the four replicate fitness measures that sexual selection promoted adaptation. In addition, a comparison of fitness measures conducted under different mating environments demonstrated a significant direct cost of sexual selection to females, likely arising from some form of male-induced harm. Indirect benefits of sexual selection in promoting adaptation to this novel resource environment therefore appear to be absent in this species, despite prior evidence suggesting the operation of good-genes mate choice in their ancestral environment. How novel environments affect the operation of good-genes mate choice is a fundamental question for future sexual selection research.
The mating preferences of female seaweed flies Coelopa frigida were determined by observing their acceptance or rejection of males of known size. The inversion karyotype of both males and females was also determined. Females exhibited a preference to mate with large males, and evidence is presented that a genetic correlation exists between the female preference and the preferred trait. Females carrying the inversion karyotype associated with large male size showed a strong preference for large males; females carrying the inversion associated with small male size also exhibited a preference for large males, but it was significantly less strong. This finding suggests that a Fisherian process may be operating.
Everything VariesSignificanceGood and Bad HypothesesNull Hypothesesp ValuesInterpretationStatistical ModellingMaximum LikelihoodExperimental DesignThe Principle of Parsimony (Occam's Razor)Observation, Theory and ExperimentControlsReplication: It's the n's that Justify the MeansHow Many Replicates?PowerRandomizationStrong InferenceWeak InferenceHow Long to Go On?PseudoreplicationInitial ConditionsOrthogonal Designs and Non-orthogonal Observational Data
The effect of indirect sexual selection on offspring fitness with
respect to a large chromosomal inversion system was estimated in nine
widely separated populations of the seaweed fly, Coelopa frigida. The
pattern of female rejection was determined for each population and
estimates were made of the relative fitnesses of the inversion
karyotypes. Two sets of progeny frequencies were calculated: the first
on the basis of the observed pattern of mating, and the second on the
hypothetical basis that all females had accepted the male available: in
other words, random mating. The relative fitnesses of the offspring
produced by these two mating regimes were compared. In seven of the
populations the exercise of choice resulted in a modest change in
progeny fitness. The change depended on the karyotype of the female:
β β females produced fitter offspring in all populations,
α α 's usually produced less fit offspring, and there was
little effect on the progeny of α β 's. An association was
also found between a physical factor, tidal range, and the offspring
fitness of α α females, but no association exists for
α β or β β females. It is suggested that the
relevant genes have been subject to different evolutionary forces on the
two forms of the inversion.
Why have males in many species evolved more conspicuous ornaments and signals such as bright colours, enlarged fins, and feather plumes, as well as larger horns and other weapons than females? Darwin's explanation for such secondary sex traits, the theory of sexual selection, became his scientifically perhaps most controversial idea. It suggests that the traits are favoured by competition over mates. After a long period of relative quiescence, theoretical and empirical research on sexual selection has erupted during the last decades. This book describes the theory and its recent development, reviews models, methods, and empirical tests, and identifies many remaining open problems.
Among the topics discussed are the selection and evolution of mating preferences; relations between sexual selection, species recognition, and speciation; constraints on sexual selection; the selection of secondary sex differences in body size, weapons, and in visual, acoustic, and chemical signals. The rapidly growing study of sexual selection in plants is also reviewed. Other chapters deal with alternative mating tactics, and with the relationships among sexual selection, parental roles, and mating systems. The present review of this very active research field will be of interest to students, teachers, and research workers in behavioural and evolutionary ecology, animal behaviour, plant reproductive ecology, and other areas of evolutionary biology where sexual selection is a potential selection factor. In spite of much exciting progress, some of the main questions in the theory of sexual selection yet remain to be answered.
The relative contributions of the Fisher process and viability indicator mechanisms to the maintenance of a female mating preference in seaweed flies have been assessed. Both types of mechanism seem to operate, but their effectiveness varies in different populations depending on ecological factors. In stable populations not subject to tidal variation, all females prefer to mate with large males and produce large, `sexy' sons. In contrast, females from a tidal population, which suffers regular genetic bottlenecks, appear to mate disassortatively with respect to both size and a chromosomal inversion system, thereby increasing the proportion of highly fit, heterokaryotypic offspring. This relation between population stability and female preference suggests that the Fisher process may not operate in populations suffering genetic bottlenecks.
The occurrence of Coelopa was plotted around the mainland of Great Britain and was found to be made up of an irregular distributed series of colonies each centred upon a site of recurrent deposition of `wrack-beds'. The pattern of events at a single colony was observed over 2 years and a generalized description of the variability encountered in the life of the colony is given. Finally, the degree of isolation between colonies is discussed.
In spite of abundant evidence that intra- and inter-specific competition occurs in natural communities, there is surprisingly little to suggest it is a major force promoting genetic change. This report assesses the genetic effects of competition in two species of seaweed fly, Coelopa frigida and C. pilipes. In laboratory cultures of C. frigida the relative survival of heterozygotes at the Adh locus, which was being used as a marker for the large αβ chromosomal inversion, was greater than that of homozygotes. In monocultures of C. frigida this competitive superiority was dependent on larval density. At low densities facilitation was seen, whereas at high larval densities there was competition. In mixed cultures of the two species, interspecific competition contributed to the differential mortality of C. frigida, and observations of natural populations suggested that competition may have similar effects to those described in laboratory culture. A possible mechanism involving the supply of nutritive microorganisms is proposed to underly both intra- and inter-specific competition. In seaweed flies, competition and the consequent differential mortality appear to be forces maintaining rather than reducing genetic variation.
With a small effective population size, random genetic drift is more important than selection in determining the fate of new alleles. Small populations therefore accumulate deleterious mutations. Left unchecked, the effect of these fixed alleles is to reduce the reproductive capacity of a species, eventually to the point of extinction. New beneficial mutations, if fixed by selection, can restore some of this lost fitness. This paper derives the overall change in fitness due to fixation of new deleterious and beneficial alleles, as a function of the distribution of effects of new mutations and the effective population size. There is a critical effective size below which a population will on average decline in fitness, but above which beneficial mutations allow the population to persist. With reasonable estimates of the relevant parameters, this critical effective size is likely to be a few hundred. Furthermore, sexual selection can act to reduce the fixation probability of deleterious new mutations and increase the probability of fixing new beneficial mutations. Sexual selection can therefore reduce the risk of extinction of small populations.
Abstract Species that exist in heterogeneous environments experience selection for specialization that is opposed by the homogenizing forces of migration and recombination. Migration tends to reduce associations between alleles and habitats, whereas recombination tends to break down associations among loci. The idea that heterogeneity should favor the evolution of isolating mechanisms has motivated evolutionary studies of reduced migration, habitat preference, and assortative mating. However, costly female choice of high-quality males can also evolve in heterogeneous populations and is not hindered by either recombination or migration. When information on male fitness is available through indicator traits, female choice based on these traits increases associations between female choice alleles and locally adapted alleles. Not only does female choice evolve in a heterogeneous environment, it acts to enhance the level of genetic variation and is thus self-reinforcing. The amount of female choice at equilibrium depends on how well mixed the habitats are, how much information on male genotype is available, and how different the habitats are. Female choice reaches the highest levels for intermediate levels of heterogeneity, because at such levels of heterogeneity there is both a high risk and high cost of mismating.
Despite the recent explosion of interest in sexual conflict, the effect of environmental conditions on the intensity of sexual conflict within populations has been largely ignored. Reproductive encounters within coelopids are characterized by sexual conflict in the form of intense harassment by males, usually resulting in a vigorous premating struggle. We investigated the effect of habitat composition and duration of exposure to oviposition sites on the level of sexual harassment by males and mating success in two species of European seaweed flies, Coelopa frigida and C. pilipes. The wrack beds inhabited by these two species are dominated by two genera of brown algae, Fucus and Laminaria, the relative proportions of which can vary considerably between wrack beds. Fucus is known to stimulate harassment by males, increase copulation duration and induce females to oviposit in both species. In this study Laminaria stimulated a higher level of harassment by male C. frigida than Fucus did. However, a similar effect was not observed in C. pilipes, with the main additional factor affecting harassment in this species being the age of the male. Our study highlights the potential importance of environmental conditions on the intensity of sexual conflict within a population. We discuss the evolutionary significance of these observed effects in seaweed flies.
The mating system of sciomyzoid flies is typified by vigorous premating struggles and a large male mating advantage. Females commonly exhibit three behaviours (shaking, kicking and curling) during struggles. We tested the predictions of three hypotheses proposed to explain the evolution of female resistance in Coelopa frigida. Both shaking and curling were associated with reduced female mating rate and thus appear to be resistance traits. Mounts that ended while the female was curling appeared to be terminated by the male dismounting from the female rather than as a result of resistance. The communication hypothesis proposes that female resistance functions by signalling to the male that the female is unwilling to mate to encourage males to dismount them. Curling therefore seems to fit the predictions of the communication hypothesis. Shaking was associated with sexual selection for large male size and also males that could withstand resistance the longest. These observations fit with the predictions of both the female reluctance and screening hypotheses. Furthermore, shaking was associated with a pattern of mating that increased offspring fitness. This did not occur in females that did not shake. This corresponds with the predictions of the screening hypothesis that resistance generates indirect sexual selection. However, our results are also largely consistent with the female reluctance hypothesis. It appears that different resistance behaviours may have different functions, and furthermore that individual resistance behaviours might generate different mating rates and patterns of sexual selection between female karyotypes.
• In considering the Origin of Species, it is quite conceivable that a naturalist, reflecting on the mutual affinities of organic beings, on their embryological relations, their geographical distribution, geological succession, and other such facts, might come to the conclusion that each species had not been independently created, but had descended, like varieties, from other species. Nevertheless, such a conclusion, even if well founded, would be unsatisfactory, until it could be shown how the innumerable species inhabiting this world have been modified, so as to acquire that perfection of structure and coadaptation which most justly excites our admiration. Naturalists continually refer to external conditions, such as climate, food, &c, as the only possible cause of variation. In one very limited sense, as we shall hereafter see, this may be true; but it is preposterous to attribute to mere external conditions, the structure, for instance, of the woodpecker, with its feet, tail, beak, and tongue, so admirably adapted to catch insects under the bark of trees. In the case of the misseltoe, which draws its nourishment from certain trees, which has seeds that must be transported by certain birds, and which has flowers with separate sexes absolutely requiring the agency of certain insects to bring pollen from one flower to the other, it is equally preposterous to account for the structure of this parasite, with its relations to several distinct organic beings, by the effects of external conditions, or of habit, or of the volition of the plant itself. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
• In considering the Origin of Species, it is quite conceivable that a naturalist, reflecting on the mutual affinities of organic beings, on their embryological relations, their geographical distribution, geological succession, and other such facts, might come to the conclusion that each species had not been independently created, but had descended, like varieties, from other species. Nevertheless, such a conclusion, even if well founded, would be unsatisfactory, until it could be shown how the innumerable species inhabiting this world have been modified, so as to acquire that perfection of structure and coadaptation which most justly excites our admiration. Naturalists continually refer to external conditions, such as climate, food, &c, as the only possible cause of variation. In one very limited sense, as we shall hereafter see, this may be true; but it is preposterous to attribute to mere external conditions, the structure, for instance, of the woodpecker, with its feet, tail, beak, and tongue, so admirably adapted to catch insects under the bark of trees. In the case of the misseltoe, which draws its nourishment from certain trees, which has seeds that must be transported by certain birds, and which has flowers with separate sexes absolutely requiring the agency of certain insects to bring pollen from one flower to the other, it is equally preposterous to account for the structure of this parasite, with its relations to several distinct organic beings, by the effects of external conditions, or of habit, or of the volition of the plant itself. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Genotype-by-environment interactions (GxEs) in naturally selected traits have been extensively studied, but the impact of GxEs on sexual selection has only recently begun to receive attention. Here, we review recent models and consider how GxEs might affect the evolution of sexual traits through influencing sexual signal reliability and also how GxEs may influence variation in sexually selected traits and the process of reproductive isolation. We then assess the current empirical literature on GxEs in sexual selection and conclude by highlighting areas that need additional work. Research on GxEs and sexual selection is an important new area of study for the discipline, which has largely focused on relatively simple mate choice/competition scenarios to date. Investigators now need to apply this knowledge to more complex, but realistic, situations, to more fully explore the evolution of sexual traits, and in this review we suggest potentially useful directions for future research.
Coelopids live in wrack beds consisting of seaweed washed up on beaches. 5 Their mating system is characterized by sexual conflict and convenience 6 polyandry, with females resisting male mating attempts. We estimated the 7 level of harassment by males and the success rate of rejection by females 8 collected from a high density wild population. Males mounted a female every 9 8.41 min. Of these mounts 35% resulted in copulation. This suggests that 10 females could be mated up to 5 times every 2 h. Females typically live for 11 3 weeks, and thus, could mate with hundreds of males during their lifetime. 12 We found a 50:50 sex ratio throughout the wrack bed revealing that females 13 do not avoidmale harassment by leaving the wrack bed when not ovipositing.
Female mating preferences were studied in the seaweed fly, Coelopa frigida. The female acceptance/rejection response to the intial mount by randomly chosen males was scored and male mating success determined by the subsequent production of progeny. The sizes of males and females, as well as their genotypes at the alcohol dehydrogenase (Adh) locus, were determined. Both adult size and the Adh locus are known to be strongly associated with a large chromosomal inversion system. Stepwise multiple regression analyses revealed no association between male mating success and male Adh genotype, but a stong association was found with male size. Female mating preferences appear to exert strong directional selection in favour of large males. There was also an association between female acceptance rate and female Adh genotype, which is likely to be a consequence of inversion karyotype rather than the Adh locus. It is suggested that the discrepancy between the mean size of males in natural populations and the preferred male size indicates that the forces of natural (viability) selection and sexual selection act in opposition.
The rate at which the seaweed fly, Coelopa frigida, develops from egg to adult is shown to be associated with the presence of alternate alleles at the alcohol dehydrogenase locus. Evidence for this correlation is presented for animals in laboratory culture and in natural populations. The relevance of the association to the maintenance of genetic polymorphism is discussed.
Although theory indicates that indirect genetic benefits through mate choice should be widespread, empirical work has often either failed to detect the operation of such benefits or shown a net cost to the presence of sexual selection. We tested whether sexual selection can increase the speed with which a conditionally deleterious allele is removed from a laboratory population of Drosophila melanogaster. The alcohol dehydrogenase null allele (Adh-) confers slightly lower viability than wild-type alleles in the absence of ethanol but is lethal in homozygotes when ethanol comprises 6% of the medium. We tracked the frequency of this allele in artificially constructed populations reared at three different levels of ethanol (0%, 2%, and 4%) that either experienced sexual selection or did not. Loss of the deleterious Adh- allele was more rapid when sexual selection was allowed to act, especially in the presence of ethanol. We also quantified the strength of both nonsexual and sexual selection against the Adh- allele using maximum-likelihood estimation. In contrast to recent experiments employing monogamy/polygamy designs, our results demonstrate a fitness benefit to sexual selection. This is consistent with the operation of good-genes female choice.
Healthy males are likely to have higher mating success than unhealthy males because of differential expression of condition-dependent traits such as mate searching intensity, fighting ability, display vigor, and some types of exaggerated morphological characters. We therefore expect that most new mutations that are deleterious for overall fitness may also be deleterious for male mating success. From this perspective, sexual selection is not limited to influencing those genes directly involved in exaggerated morphological traits but rather affects most, if not all, genes in the genome. If true, sexual selection can be an important force acting to reduce the frequency of deleterious mutations and, as a result, mutation load. We review the literature and find various forms of indirect evidence that sexual selection helps to eliminate deleterious mutations. However, direct evidence is scant, and there are almost no data available to address a key issue: is selection in males stronger than selection in females? In addition, the total effect of sexual selection on mutation load is complicated by possible increases in mutation rate that may be attributable to sexual selection. Finally, sexual selection affects population fitness not only through mutation load but also through sexual conflict, making it difficult to empirically measure how sexual selection affects load. Several lines of enquiry are suggested to better fill large gaps in our understanding of sexual selection and its effect on genetic load.
Seaweed flies (Coelopa frigida) inhabit piles of decaying seaweed on the seashore. All populations so far studied have been found to be polymorphic at the alcohol dehydrogenase locus (Adh). This article reports an attempt to identify some of the forces of natural selection that may be maintaining this polymorphism First, the genetic determination of the rather complex isozyme system is described. Several inbred lines homozygous at the Adh locus were derived and the biochemical properties of their allozymes compared. Significant differences in both specific activities and thermal stabilities were found between ADH allozymes. A simple experiment is reported in which individuals with different Adh genotypes were cultured in competition with each other in the presence of elevated levels of ethanol. Although the presence of ethanol resulted in greater mortality, there is no evidence that it was selective with respect to the Adh genotypes. The possible relevance of these results to the maintenance of the Adh polymorphism is discussed.
Populations of seaweed fly Coelopa frigida are polymorphic at three loci determining the enzymes peptidase-1 (Pep-1), alcohol dehydrogenase (Adh) and larval esterase-2 (Es-2). Alleles at these loci have been shown by others to be non-randomly associated with each other. In the present paper we report non-random associations between the Adh and Es-2 loci and inversions on chromosome I. The two common alleles Adh-B and D are in strong linkage disequilibrium with the alpha and beta inversions, but the Adh-A and C alleles are not so. The X and Y alleles at the Es-2 locus show weak, but still significant, associations with the inversions. We consider possible linkage relationships of the loci on the chromosomal arrangements, and discuss the hypothesis that they constitute part of a coadapted gene complex whose members code for functionally related enzymes.
The mating system of the seaweed fly involves a premating struggle. When mounted, females violently try to remove the male. In this study 48% of premating struggles resulted in successful rejection of the male, 46% in copulation and 6% were terminated by the male. Large males had a mating advantage. However, contrary to what would be predicted if this sexual selection occurred as a result of active female mate choice, we found a positive association between the duration of premating struggles and male size. A positive association was also found between the duration of premating struggles and male mating success, suggesting that large males may benefit through their superior ability to withstand female rejection. Large females rejected males more easily than small females, suggesting that the premating struggle has not evolved to allow mate assessment by females. We conclude that sexual selection is occurring as a side-effect of the female rejection response, which has probably evolved in order to avoid costs associated with copulation. Nevertheless, a sexual size dimorphism has evolved with males being larger and much more variable in size than females. (c) 1998 The Association for the Study of Animal Behaviour.
With a small effective population size, random genetic drift is more important than selection in determining the fate of new alleles. Small populations therefore accumulate deleterious mutations. Left unchecked, the effect of these fixed alleles is to reduce the reproductive capacity of a species, eventually to the point of extinction. New beneficial mutations, if fixed by selection, can restore some of this lost fitness. This paper derives the overall change in fitness due to fixation of new deleterious and beneficial alleles, as a function of the distribution of effects of new mutations and the effective population size. There is a critical effective size below which a population will on average decline in fitness, but above which beneficial mutations allow the population to persist. With reasonable estimates of the relevant parameters, this critical effective size is likely to be a few hundred. Furthermore, sexual selection can act to reduce the fixation probability of deleterious new mutations and increase the probability of fixing new beneficial mutations. Sexual selection can therefore reduce the risk of extinction of small populations.
Species that exist in heterogeneous environments experience selection for specialization that is opposed by the homogenizing forces of migration and recombination. Migration tends to reduce associations between alleles and habitats, whereas recombination tends to break down associations among loci. The idea that heterogeneity should favor the evolution of isolating mechanisms has motivated evolutionary studies of reduced migration, habitat preference, and assortative mating. However, costly female choice of high-quality males can also evolve in heterogeneous populations and is not hindered by either recombination or migration. When information on male fitness is available through indicator traits, female choice based on these traits increases associations between female choice alleles and locally adapted alleles. Not only does female choice evolve in a heterogeneous environment, it acts to enhance the level of genetic variation and is thus self-reinforcing. The amount of female choice at equilibrium depends on how well mixed the habitats are, how much information on male genotype is available, and how different the habitats are. Female choice reaches the highest levels for intermediate levels of heterogeneity, because at such levels of heterogeneity there is both a high risk and high cost of mismating.
Selection can be divided into sexual and nonsexual components. Some work finds that a component of sexual selection, adaptive female selection for good genes, can promote nonsexual fitness. Less studied is the benefit from sexual selection in toto, that is, when intra- and intersexual selection are both present and able to affect females directly and indirectly. Here an upper bound for the net benefit of sexual selection is estimated for Drosophila melanogaster. Replicate populations were allowed to adapt to low-grade thermal stress, with or with out the operation of sexual selection. Because proteins and lipids are highly sensitive to temperature, low-grade thermal stress will select broadly across the genome for alternative alleles. Such broad, directional selection for thermal tolerance should increase the measurable benefits of sexual selection far beyond that available under stabilizing selection. Sexual selection was removed by enforced monogamy without mate choice and retained by enforced polyandry (four males per female). After 36 generations of thermal stress exposure, there was substantial adaptation to the new environment (the net reproductive rate increased six standard deviations relative to thermal controls). However, sexual selection did not affect the rate of adaptation. Therefore, adaptive female selection for thermal tolerance either was insignificant or negated by other aspects of sexual selection, for example, male-induced female harm, which has been shown to diminish under monogamy. This experiment employed two parameters that reduced the opportunity for divergence in such harm: a truncated intersexual interaction period and strong directional selection for thermal tolerance. No divergence in male-induced harm was observed.
The net effect of sexual selection on nonsexual fitness is controversial. On one side, elaborate display traits and preferences for them can be costly, reducing the nonsexual fitness of individuals possessing them, as well as their offspring. In contrast, sexual selection may reinforce nonsexual fitness if an individual's attractiveness and quality are genetically correlated. According to recent models, such good-genes mate choice should increase both the extent and rate of adaptation. We evolved 12 replicate populations of Drosophila serrata in a powerful two-way factorial experimental design to test the separate and combined contributions of natural and sexual selection to adaptation to a novel larval food resource. Populations evolving in the presence of natural selection had significantly higher mean nonsexual fitness when measured over three generations (13-15) during the course of experimental evolution (16-23% increase). The effect of natural selection was even more substantial when measured in a standardized, monogamous mating environment at the end of the experiment (generation 16; 52% increase). In contrast, and despite strong sexual selection on display traits, there was no evidence from any of the four replicate fitness measures that sexual selection promoted adaptation. In addition, a comparison of fitness measures conducted under different mating environments demonstrated a significant direct cost of sexual selection to females, likely arising from some form of male-induced harm. Indirect benefits of sexual selection in promoting adaptation to this novel resource environment therefore appear to be absent in this species, despite prior evidence suggesting the operation of good-genes mate choice in their ancestral environment. How novel environments affect the operation of good-genes mate choice is a fundamental question for future sexual selection research.
Statistics: an introduction using R Sexual selection as a side-effect of sexual conflict in the seaweed fly, Coelopa ursina (Diptera : Coelopidae)
- M J Crawley
Crawley, M. J. 2005. Statistics: an introduction using R. John Wiley & Sons, Chichester. Crean, C. S., and A. S. Gilburn. 1998. Sexual selection as a side-effect of sexual conflict in the seaweed fly, Coelopa ursina (Diptera : Coelopidae). Anim. Behav. 56:1405–1410.
On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life Alcohol dehydrogenase polymorphism in the seaweed fly, Coelopa frigida
- C Darwin
- John Murray
- London
- T H Day
- P A Buckley
Darwin, C. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, London. Day, T. H., and P. A. Buckley. 1980. Alcohol dehydrogenase polymorphism in the seaweed fly, Coelopa frigida. Biochem. Genet. 18:727–741.
- Darwin