Adaptive variation in environmental and genetic sex determination in a fish

Two general mechanisms of sex determination have been identified among gonochoristic vertebrates: environmental sex determination where offspring become male or female in response to an environmental factor(s) during development (for example, some fishes and reptiles); and genetic sex determination where sex is determined by genotype at conception (as in birds and mammals). How do these sex-determining systems evolve? Direct evidence is virtually non-existent because the sex-determining systems of most species appear to have little genetic variation. Here we provide the first evidence of adaptive variation in environmental and genetic sex determination within a species. We show that in a fish with temperature-dependent sex determination, populations at different latitudes compensate for differences in thermal environment and seasonality by adjusting the response of sex ratio to temperature, and by altering the level of environmental as opposed to genetic control. The adjustments observed are precisely those predicted by adaptive sex ratio theory.     

Turnover of sex chromosomes induced by sexual conflict

Sex-determination genes are among the most fluid features of the genome in many groups of animals. In some taxa the master sex-determining gene moves frequently between chromosomes, whereas in other taxa different genes have been recruited to determine the sex of the zygotes. There is a well developed theory for the origin of stable and highly dimorphic sex chromosomes seen in groups such as the eutherian mammals. In contrast, the evolutionary lability of genetic sex determination in other groups remains largely unexplained. In this theoretical study, we show that an autosomal gene under sexually antagonistic selection can cause the spread of a new sex-determining gene linked to it. The mechanism can account for the origin of new sex-determining loci, the transposition of an ancestral sex-determining gene to an autosome, and the maintenance of multiple sex-determining factors in species that lack heteromorphic sex chromosomes.     

Evolution driven by differential dispersal within a wild bird population

Evolutionary theory predicts that local population divergence will depend on the balance between the diversifying effect of selection and the homogenizing effect of gene flow. However, spatial variation in the expression of genetic variation will also generate differential evolutionary responses. Furthermore, if dispersal is non-random it may actually reinforce, rather than counteract, evolutionary differentiation. Here we document the evolution of differences in body mass within a population of great tits, Parus major, inhabiting a single continuous woodland, over a 36-year period. We show that genetic variance for nestling body mass is spatially variable, that this generates different potential responses to selection, and that this diversifying effect is reinforced by non-random dispersal. Matching the patterns of variation, selection and evolution with population ecological data, we argue that the small-scale differentiation is driven by density-related differences in habitat quality affecting settlement decisions. Our data show that when gene flow is not homogeneous, evolutionary differentiation can be rapid and can occur over surprisingly small spatial scales. Our findings have important implications for questions of the scale of adaptation and speciation, and challenge the usual treatment of dispersal as a force opposing evolutionary differentiation.     

The adaptive significance of temperature-dependent sex determination in a reptile

Understanding the mechanisms that determine an individual's sex remains a primary challenge for evolutionary biology. Chromosome-based systems (genotypic sex determination) that generate roughly equal numbers of sons and daughters accord with theory, but the adaptive significance of environmental sex determination (that is, when embryonic environmental conditions determine offspring sex, ESD) is a major unsolved problem. Theoretical models predict that selection should favour ESD over genotypic sex determination when the developmental environment differentially influences male versus female fitness (that is, the Charnov-Bull model), but empirical evidence for this hypothesis remains elusive in amniote vertebrates--the clade in which ESD is most prevalent. Here we provide the first substantial empirical support for this model by showing that incubation temperatures influence reproductive success of males differently than that of females in a short-lived lizard (Amphibolurus muricatus, Agamidae) with temperature-dependent sex determination. We incubated eggs at a variety of temperatures, and de-confounded sex and incubation temperature by using hormonal manipulations to embryos. We then raised lizards in field enclosures and quantified their lifetime reproductive success. Incubation temperature affected reproductive success differently in males versus females in exactly the way predicted by theory: the fitness of each sex was maximized by the incubation temperature that produces that sex. Our results provide unequivocal empirical support for the Charnov-Bull model for the adaptive significance of temperature-dependent sex determination in amniote vertebrates.     

同域培养下大肠杆菌氮、磷含量的进化趋异研究

利用9株具有不同进化背景的大肠杆菌构成5个短期可竞争共存的祖先配对,在限制氮、磷资源的环境下,对5个进化组下6个重复家系进行了约1 100世代的选择实验,考察了这些细菌在进化前后菌体氮、磷质量分数w的变化,并评估了这些性状的趋异程度.研究发现:后代细菌w(氮)的变动范围在13.1%~14.2%,而w(磷)为1.70%~1.95%;不同进化组内,细菌氮、磷含量改变的模式不同;同域后代细菌的趋异模式也并不相同.推测细菌进化本身可能会产生许多独特的性状,连同生态相互作用一起,增加了结果的复杂性,需要在更精细的水平上寻找产生这种结果的原因.     

Speciation in a ring

The evolutionary divergence of a single species into two has never been directly observed in nature, primarily because speciation can take a long time to occur. A ring species, in which a chain of intergrading populations encircles a barrier and the terminal forms coexist without interbreeding, provides a situation in which variation in space can be used to infer variation in time. Here we reconstruct the pathway to speciation between two reproductively isolated forms of greenish warbler (Phylloscopus trochiloides). These two taxa do not interbreed in central Siberia but are connected by a long chain of intergrading populations encircling the Tibetan Plateau to the south. Molecular data and climatic history imply that the reproductively isolated taxa came into contact following expansions northward around the western and eastern sides of the plateau. Parallel selection pressures for increased song complexity during the northward expansions have been accompanied by divergence in song structure. Playback experiments show that the two Siberian forms do not recognize each other's songs. Our results show how gradual divergence in a trait involved in mate choice leads to the formation of new species.     

Sexual dimorphism and adaptive radiation in Anolis lizards

Sexual dimorphism is widespread and substantial throughout the animal world. It is surprising, then, that such a pervasive source of biological diversity has not been integrated into studies of adaptive radiation, despite extensive and growing attention to both phenomena. Rather, most studies of adaptive radiation either group individuals without regard to sex or focus solely on one sex. Here we show that sexual differences contribute substantially to the ecomorphological diversity produced by the adaptive radiations of West Indian Anolis lizards: within anole species, males and females occupy mostly non-overlapping parts of morphological space; the overall extent of sexual variation is large relative to interspecific variation; and the degree of variation depends on ecological type. Thus, when sexual dimorphism in ecologically relevant traits is substantial, ignoring its contribution may significantly underestimate the adaptive component of evolutionary radiation. Conversely, if sexual dimorphism and interspecific divergence are alternative means of ecological diversification, then the degree of sexual dimorphism may be negatively related to the extent of adaptive radiation.     

Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila

Spontaneous mutations are the source of genetic variation required for evolutionary change, and are therefore important for many aspects of evolutionary biology. For example, the divergence between taxa at neutrally evolving sites in the genome is proportional to the per nucleotide mutation rate, u (ref. 1), and this can be used to date speciation events by assuming a molecular clock. The overall rate of occurrence of deleterious mutations in the genome each generation (U) appears in theories of nucleotide divergence and polymorphism, the evolution of sex and recombination, and the evolutionary consequences of inbreeding. However, estimates of U based on changes in allozymes or DNA sequences and fitness traits are discordant. Here we directly estimate u in Drosophila melanogaster by scanning 20 million bases of DNA from three sets of mutation accumulation lines by using denaturing high-performance liquid chromatography. From 37 mutation events that we detected, we obtained a mean estimate for u of 8.4 x 10(-9) per generation. Moreover, we detected significant heterogeneity in u among the three mutation-accumulation-line genotypes. By multiplying u by an estimate of the fraction of mutations that are deleterious in natural populations of Drosophila, we estimate that U is 1.2 per diploid genome. This high rate suggests that selection against deleterious mutations may have a key role in explaining patterns of genetic variation in the genome, and help to maintain recombination and sexual reproduction.     

Niche lability in the evolution of a Caribbean lizard community

Niche conservatism--the tendency for closely related species to be ecologically similar--is widespread. However, most studies compare closely related taxa that occur in allopatry; in sympatry, the stabilizing forces that promote niche conservatism, and thus inhibit niche shifts, may be countered by natural selection favouring ecological divergence to minimize the intensity of interspecific interactions. Consequently, the relative importance of niche conservatism versus niche divergence in determining community structure has received little attention. Here, we examine a tropical lizard community in which species have a long evolutionary history of ecological interaction. We find that evolutionary divergence overcomes niche conservatism: closely related species are no more ecologically similar than expected by random divergence and some distantly related species are ecologically similar, leading to a community in which the relationship between ecological similarity and phylogenetic relatedness is very weak. Despite this lack of niche conservatism, the ecological structuring of the community has a phylogenetic component: niche complementarity only occurs among distantly related species, which suggests that the strength of ecological interactions among species may be related to phylogeny, but it is not necessarily the most closely related species that interact most strongly.     

Testis determination requires insulin receptor family function in mice

In mice, gonads are formed shortly before embryonic day 10.5 by the thickening of the mesonephros and consist of somatic cells and migratory primordial germ cells. The male sex-determining process is set in motion by the sex-determining region of the Y chromosome (Sry), which triggers differentiation of the Sertoli cell lineage. In turn, Sertoli cells function as organizing centres and direct differentiation of the testis. In the absence of Sry expression, neither XX nor XY gonads develop testes, and alterations in Sry expression are often associated with abnormal sexual differentiation. The molecular signalling mechanisms by which Sry specifies the male pathway and models the undifferentiated gonad are unknown. Here we show that the insulin receptor tyrosine kinase family, comprising Ir, Igf1r and Irr, is required for the appearance of male gonads and thus for male sexual differentiation. XY mice that are mutant for all three receptors develop ovaries and show a completely female phenotype. Reduced expression of both Sry and the early testis-specific marker Sox9 indicates that the insulin signalling pathway is required for male sex determination.     

Divergent sexual selection enhances reproductive isolation in sticklebacks

Sexual selection may facilitate speciation because it can cause rapid evolutionary diversification of male mating signals and female preferences. Divergence in these traits can then contribute to reproductive isolation. The sensory drive hypothesis predicts that three mechanisms underlie divergence in sexually selected traits: (1) habitat-specific transmission of male signals; (2) adaptation of female perceptual sensitivity to local ecological conditions; and (3) matching of male signals to female perceptual sensitivity. I test these mechanisms in threespine sticklebacks (Gasterosteus spp.) that live in different light environments. Here I show that female perceptual sensitivity to red light varies with the extent of redshift in the light environment, and contributes to divergent preferences. Male nuptial colour varies with environment and is tuned to female perceptual sensitivity. The extent of divergence among populations in both male signal colour and female preference for red is correlated with the extent of reproductive isolation in these recently diverged species. These results demonstrate that divergent sexual selection generated by sensory drive contributes to speciation.     

Sex increases the efficacy of natural selection in experimental yeast populations

Why sex evolved and persists is a problem for evolutionary biology, because sex disrupts favourable gene combinations and requires an expenditure of time and energy. Further, in organisms with unequal-sized gametes, the female transmits her genes at only half the rate of an asexual equivalent (the twofold cost of sex). Many modern theories that provide an explanation for the advantage of sex incorporate an idea originally proposed by Weismann more than 100 years ago: sex allows natural selection to proceed more effectively because it increases genetic variation. Here we test this hypothesis, which still lacks robust empirical support, with the use of experiments on yeast populations. Capitalizing on recent advances in the molecular biology of recombination in yeast, we produced by genetic manipulation strains that differed only in their capacity for sexual reproduction. We show that, as predicted by the theory, sex increases the rate of adaptation to a new harsh environment but has no measurable effect on fitness in a new benign environment where there is little selection.     

Sex releases the speed limit on evolution

Explaining the evolutionary maintenance of sex remains a key problem in evolutionary biology. One potential benefit of sex is that it may allow a more rapid adaptive response when environmental conditions change, by increasing the efficiency with which selection can fix beneficial mutations. Here I show that sex can increase the rate of adaptation in the facultatively sexual single-celled chlorophyte Chlamydomonas reinhardtii, but that the benefits of sex depend crucially on the size of the population that is adapting: sex has a marked effect in large populations but little effect in small populations. Several mechanisms have been proposed to explain the benefits of sex in a novel environment, including stochastic effects in small populations, clonal interference and epistasis between beneficial alleles. These results indicate that clonal interference is important in this system.     

Genetic evidence equating SRY and the testis-determining factor

The testis-determining factor gene (TDF) lies on the Y chromosome and is responsible for initiating male sex determination. SRY is a gene located in the sex-determining region of the human and mouse Y chromosomes and has many of the properties expected for TDF. Sex reversal in XY females results from the failure of the testis determination or differentiation pathways. Some XY females, with gonadal dysgenesis, have lost the sex-determining region from the Y chromosome by terminal exchange between the sex chromosomes or by other deletions. If SRY is TDF, it would be predicted that some sex-reversed XY females, without Y chromosome deletions, will have suffered mutations in SRY. We have tested human XY females and normal XY males for alterations in SRY using the single-strand conformation polymorphism assay and subsequent DNA sequencing. A de novo mutation was found in the SRY gene of one XY female: this mutation was not present in the patient's normal father and brother. A second variant was found in the SRY gene of another XY female, but in this case the normal father shared the same alteration. The variant in the second case may be fortuitously associated with, or predisposing towards sex reversal; the de novo mutation associated with sex reversal provides compelling evidence that SRY is required for male sex determination.     

Developmental constraints versus flexibility in morphological evolution

Evolutionary developmental biology has encouraged a change of research emphasis from the sorting of phenotypic variation by natural selection to the production of that variation through development. Some morphologies are more readily generated than others, and developmental mechanisms can limit or channel evolutionary change. Such biases determine how readily populations are able to respond to selection, and have been postulated to explain stasis in morphological evolution and unexplored morphologies. There has been much discussion about evolutionary constraints but empirical data testing them directly are sparse. The spectacular diversity in butterfly wing patterns is suggestive of how little constrained morphological evolution can be. However, for wing patterns involving serial repeats of the same element, developmental properties suggest that some directions of evolutionary change might be restricted. Here we show that despite the developmental coupling between different eyespots in the butterfly Bicyclus anynana, there is great potential for independent changes. This flexibility is consistent with the diversity of wing patterns across species and argues for a dominant role of natural selection, rather than internal constraints, in shaping existing variation.     

Why large-scale climate indices seem to predict ecological processes better than local weather

Large-scale climatic indices such as the North Atlantic Oscillation are associated with population dynamics, variation in demographic rates and values of phenotypic traits in many species. Paradoxically, these large-scale indices can seem to be better predictors of ecological processes than local climate. Using detailed data from a population of Soay sheep, we show that high rainfall, high winds or low temperatures at any time during a 3-month period can cause mortality either immediately or lagged by a few days. Most measures of local climate used by ecologists fail to capture such complex associations between weather and ecological process, and this may help to explain why large-scale, seasonal indices of climate spanning several months can outperform local climatic factors. Furthermore, we show why an understanding of the mechanism by which climate influences population ecology is important. Through simulation we demonstrate that the timing of bad weather within a period of mortality can have an important modifying influence on intraspecific competition for food, revealing an interaction between climate and density dependence that the use of large-scale climatic indices or inappropriate local weather variables might obscure.     

Speciation through sensory drive in cichlid fish

Theoretically, divergent selection on sensory systems can cause speciation through sensory drive. However, empirical evidence is rare and incomplete. Here we demonstrate sensory drive speciation within island populations of cichlid fish. We identify the ecological and molecular basis of divergent evolution in the cichlid visual system, demonstrate associated divergence in male colouration and female preferences, and show subsequent differentiation at neutral loci, indicating reproductive isolation. Evidence is replicated in several pairs of sympatric populations and species. Variation in the slope of the environmental gradients explains variation in the progress towards speciation: speciation occurs on all but the steepest gradients. This is the most complete demonstration so far of speciation through sensory drive without geographical isolation. Our results also provide a mechanistic explanation for the collapse of cichlid fish species diversity during the anthropogenic eutrophication of Lake Victoria.     

Climatic influence on a marine fish assemblage

Understanding the fluctuations in marine fish stocks is important for the management of fisheries, and attempts have been made to demonstrate links with oceanographic and climatic variability, including the North Atlantic Oscillation (NAO). The NAO has been correlated with a range of long-term ecological measures, including certain fish stocks. Such environmental influences are most likely to affect susceptible juveniles during estuarine residency, as estuaries are critical juvenile nursery or over-wintering habitats. Here we show that, during a 16-year period, climatic forcing (by means of the NAO) is consistently the most important parameter explaining variation in assemblage composition, abundance and growth of juvenile marine fish during estuarine residency. A possible mechanism for the effect of the NAO is a temperature differential between estuarine and marine waters that allows fish to facultatively exploit optimal thermal habitats. The connection has potentially important implications for the size and numbers of individuals recruited to the fishery, for understanding and predicting the composition of juvenile fish stocks using estuaries, and for the appropriate conservation of estuarine systems in relation to fish stocks.