Natural selection commonly drives the origin of species, as Darwin initially claimed. Mechanisms of speciation by selection fall into two broad categories: ecological and mutation-order. Under ...ecological speciation, divergence is driven by divergent natural selection between environments, whereas under mutation-order speciation, divergence occurs when different mutations arise and are fixed in separate populations adapting to similar selection pressures. Tests of parallel evolution of reproductive isolation, trait-based assortative mating, and reproductive isolation by active selection have demonstrated that ecological speciation is a common means by which new species arise. Evidence for mutation-order speciation by natural selection is more limited and has been best documented by instances of reproductive isolation resulting from intragenomic conflict. However, we still have not identified all aspects of selection, and identifying the underlying genes for reproductive isolation remains challenging.
Genetics and ecological speciation Schluter, Dolph; Conte, Gina L
Proceedings of the National Academy of Sciences - PNAS,
06/2009, Letnik:
106, Številka:
Supplement 1
Journal Article
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Species originate frequently by natural selection. A general mechanism by which this occurs is ecological speciation, defined as the evolution of reproductive isolation between populations as a ...result of ecologically-based divergent natural selection. The alternative mechanism is mutation-order speciation in which populations fix different mutations as they adapt to similar selection pressures. Although numerous cases now indicate the importance of ecological speciation in nature, very little is known about the genetics of the process. Here, we summarize the genetics of premating and postzygotic isolation and the role of standing genetic variation in ecological speciation. We discuss the role of selection from standing genetic variation in threespine stickleback (Gasterosteus aculeatus), a complex of species whose ancestral marine form repeatedly colonized and adapted to freshwater environments. We propose that ecological speciation has occurred multiple times in parallel in this group via a "transporter" process in which selection in freshwater environments repeatedly acts on standing genetic variation that is maintained in marine populations by export of freshwater-adapted alleles from elsewhere in the range. Selection from standing genetic variation is likely to play a large role in ecological speciation, which may partly account for its rapidity.
Evolution generates a remarkable breadth of living forms, but many traits evolve repeatedly, by mechanisms that are still poorly understood. A classic example of repeated evolution is the loss of ...pelvic hindfins in stickleback fish (
). Repeated pelvic loss maps to recurrent deletions of a pelvic enhancer of the
gene. Here, we identify molecular features contributing to these recurrent deletions.
enhancer sequences form alternative DNA structures in vitro and increase double-strand breaks and deletions in vivo. Enhancer mutability depends on DNA replication direction and is caused by TG-dinucleotide repeats. Modeling shows that elevated mutation rates can influence evolution under demographic conditions relevant for sticklebacks and humans. DNA fragility may thus help explain why the same loci are often used repeatedly during parallel adaptive evolution.
Does competition influence patterns of coexistence between closely related taxa? Here we address this question by analyzing patterns of range overlap between related species of birds (‘sister pairs’) ...co‐occurring on a tropical elevational gradient. We explicitly contrast the behavioral dimension of interspecific competition (interference competition) with similarity in resource acquisition traits (exploitative competition). Specifically, we ask whether elevational range overlap in 118 sister pairs that live along the Manu Transect in southeastern Peru is predicted by proxies for competition (intraspecific territorial behavior) or niche divergence (beak divergence and divergence times, an estimate of evolutionary age). We find that close relatives that defend year‐round territories tend to live in non‐overlapping elevational distributions, while close relatives that do not defend territories tend to broadly overlap in elevational distribution. In contrast, neither beak divergence nor evolutionary age was associated with patterns of range limitation. We interpret these findings as evidence that behavioral interactions – particularly direct territorial aggression – can be important in setting elevational range limits and preventing coexistence of closely related species, though this depends upon the extent to which intraspecific territorial behavior can be extended to territorial interactions between species. Our results suggest that interference competition can be an important driver of species range limits in diverse assemblages, and thus highlight the importance of considering behavioral dimensions of the niche in macroecological studies.
Although the tropics harbor greater numbers of species than do temperate zones, it is not known whether the rates of speciation and extinction also follow a latitudinal gradient. By sampling birds ...and mammals, we found that the distribution of the evolutionary ages of sister species--pairs of species in which each is the other's closest relative--adheres to a latitudinal gradient. The time to divergence for sister species is shorter at high latitudes and longer in the tropics. Birth-death models fitting these data estimate that the highest recent speciation and extinction rates occur at high latitudes and decline toward the tropics. These results conflict with the prevailing view that links high tropical diversity to elevated tropical speciation rates. Instead, our findings suggest that faster turnover at high latitudes contributes to the latitudinal diversity gradient.
I give an overview of the observational and experimental evidence for ecological character displacement in adaptive radiation. Sixty‐one published cases of character displacement involving closely ...related species (congeners) make up the observational data set. All cases involve divergence, even though parallel and convergent displacement are theoretically possible. Character ratios in sympatry were greatest when displacement was symmetric (mean 1.54) and least when asymmetric (mean 1.29), perhaps because the most symmetric resource distributions are also the broadest. Carnivores are vastly overrepresented in the data compared with other trophic groups, with herbivores the next most common category. I consider five hypotheses to explain this pattern, including the possibility that the likelihood of divergence via competition depends on position in food webs. Overall, the quality and completeness of observational data has improved in recent years, as judged by the extent to which individual cases satisfy six standard criteria. All but one of the criteria are met in over half the cases. Most often lacking is independent evidence that the species involved compete for resources. For this reason, we cannot be sure that divergence in sympatry is usually the result of resource competition rather than some other interaction. Field experiments on character displacement, which explore how interaction strength changes per unit change in phenotypic traits, are only just beginning. I summarize research on threespine sticklebacks that used experiments in ponds to test three predictions: that present‐day differences between sympatric species are a “ghost” of competition past; that adding a competitor alters natural selection pressures on a species already present, favoring divergence; and that divergent natural selection stemming from resource competition is frequency dependent. In total, the evidence suggests that character displacement occurs frequently in nature, and it probably plays an important role in the evolution of diversity in many adaptive radiations.
Speciation is the process by which barriers to gene flow evolve between populations. Although we now know that speciation is largely driven by natural selection, knowledge of the agents of selection ...and the genetic and genomic mechanisms that facilitate divergence is required for a satisfactory theory of speciation. In this essay, we highlight three advances/problems in our understanding of speciation that have arisen from studies of the genes and genomic regions that underlie the evolution of reproductive isolation. First, we describe how the identification of “speciation” genes makes it possible to identify the agents of selection causing the evolution of reproductive isolation, while also noting that the link between the genetics of phenotypic divergence and intrinsic postzygotic reproductive barriers remains tenuous. Second, we discuss the important role of recombination suppressors in facilitating speciation with gene flow, but point out that the means and timing by which reproductive barriers become associated with recombination cold spots remains uncertain. Third, we establish the importance of ancient genetic variation in speciation, although we argue that the focus of speciation studies on evolutionarily young groups may bias conclusions in favor of ancient variation relative to new mutations.
Genomic and genetic methods allow investigation of how frequently the same genes are used by different populations during adaptive evolution, yielding insights into the predictability of evolution at ...the genetic level. We estimated the probability of gene reuse in parallel and convergent phenotypic evolution in nature using data from published studies. The estimates are surprisingly high, with mean probabilities of 0.32 for genetic mapping studies and 0.55 for candidate gene studies. The probability declines with increasing age of the common ancestor of compared taxa, from about 0.8 for young nodes to 0.1–0.4 for the oldest nodes in our study. Probability of gene reuse is higher when populations begin from the same ancestor (genetic parallelism) than when they begin from divergent ancestors (genetic convergence). Our estimates are broadly consistent with genomic estimates of gene reuse during repeated adaptation to similar environments, but most genomic studies lack data on phenotypic traits affected. Frequent reuse of the same genes during repeated phenotypic evolution suggests that strong biases and constraints affect adaptive evolution, resulting in changes at a relatively small subset of available genes. Declines in the probability of gene reuse with increasing age suggest that these biases diverge with time.
Biotic interactions are potent, widespread causes of natural selection and divergent phenotypic evolution and can lead to genetic differentiation with gene flow among wild populations (“isolation by ...ecology”) 1–4. Biotic selection has been predicted to act on more genes than abiotic selection thereby driving greater adaptation 5. However, difficulties in isolating the genome-wide effect of single biotic agents of selection have limited our ability to identify and quantify the number and type of genetic regions responding to biotic selection 6–9. We identified geographically interspersed lakes in which threespine stickleback fish (Gasterosteus aculeatus) have repeatedly adapted to the presence or absence of a single member of the ecological community, prickly sculpin (Cottus asper), a fish that is both a competitor and a predator of the stickleback 10. Whole-genome sequencing revealed that sculpin presence or absence accounted for the majority of genetic divergence among stickleback populations, more so than geography. The major axis of genomic variation within and between the two lake types was correlated with multiple traits, indicating parallel natural selection across a gradient of biotic environments. A large proportion of the genome—about 1.8%, encompassing more than 600 genes—differentiated stickleback from the two biotic environments. Divergence occurred in 141 discrete genomic clumps located mainly in regions of low recombination, suggesting that genes brought to lakes by the colonizing ancestral population often evolved together in linked blocks. Strong selection and a wealth of standing genetic variation explain how a single member of the biotic community can have such a rapid and profound evolutionary impact.
•Biotic selection correlated with rapid, parallel genetic differentiation•Stickleback from the two biotic environments differed in about 600 genes•There are about 140 discrete genomic regions potentially under biotic selection•Genetic differentiation correlated with variation in morphology
Miller et al. analyze genetic differentiation in wild populations of threespine stickleback fish in response to a single agent of biotic selection, intraguild predation by prickly sculpin. Sculpin presence was correlated with parallel, widespread genetic divergence. Ecological interactions between these species had large evolutionary consequences.
Evolutionary hypotheses to explain the greater numbers of species in the tropics than the temperate zone include greater age and area, higher temperature and metabolic rates, and greater ecological ...opportunity. These ideas make contrasting predictions about the relationship between speciation processes and latitude, which I elaborate and evaluate. Available data suggest that per capita speciation rates are currently highest in the temperate zone and that diversification rates (speciation minus extinction) are similar between latitudes. In contrast, clades whose oldest analyzed dates precede the Eocene thermal maximum, when the extent of the tropics was much greater than today, tend to show highest speciation and diversification rates in the tropics. These findings are consistent with age and area, which is alone among hypotheses in predicting a time trend. Higher recent speciation rates in the temperate zone than the tropics suggest an additional response to high ecological opportunity associated with low species diversity. These broad patterns are compelling but provide limited insights into underlying mechanisms, arguing that studies of speciation processes along the latitudinal gradient will be vital. Using threespine stickleback in depauperate northern lakes as an example, I show how high ecological opportunity can lead to rapid speciation. The results support a role for ecological opportunity in speciation, but its importance in the evolution of the latitudinal gradient remains uncertain. I conclude that per capita evolutionary rates are no longer higher in the tropics than the temperate zone. Nevertheless, the vast numbers of species that have already accumulated in the tropics ensure that total rate of species production remains highest there. Thus, tropical evolutionary momentum helps to perpetuate the steep latitudinal biodiversity gradient.
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