Limits...
A genetically explicit model of speciation by sensory drive within a continuous population in aquatic environments.

Kawata M, Shoji A, Kawamura S, Seehausen O - BMC Evol. Biol. (2007)

Bottom Line: In addition, our results predict that mutations that cause large shifts in the wavelength of peak absorption promote speciation, whereas we did not observe speciation when peak absorption evolved by stepwise mutations with small effect.The results suggest that speciation can occur where environmental gradients create divergent selection on sensory modalities that are used in mate choice.Evidence for such gradients exists from several animal groups, and from freshwater and marine fishes in particular.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Graduate School of Sciences, Tohoku University, Sendai, Japan. kawata@mail.tains.tohoku.ac.jp

ABSTRACT

Background: The sensory drive hypothesis predicts that divergent sensory adaptation in different habitats may lead to premating isolation upon secondary contact of populations. Speciation by sensory drive has traditionally been treated as a special case of speciation as a byproduct of adaptation to divergent environments in geographically isolated populations. However, if habitats are heterogeneous, local adaptation in the sensory systems may cause the emergence of reproductively isolated species from a single unstructured population. In polychromatic fishes, visual sensitivity might become adapted to local ambient light regimes and the sensitivity might influence female preferences for male nuptial color. In this paper, we investigate the possibility of speciation by sensory drive as a byproduct of divergent visual adaptation within a single initially unstructured population. We use models based on explicit genetic mechanisms for color vision and nuptial coloration.

Results: We show that in simulations in which the adaptive evolution of visual pigments and color perception are explicitly modeled, sensory drive can promote speciation along a short selection gradient within a continuous habitat and population. We assumed that color perception evolves to adapt to the modal light environment that individuals experience and that females prefer to mate with males whose nuptial color they are most sensitive to. In our simulations color perception depends on the absorption spectra of an individual's visual pigments. Speciation occurred most frequently when the steepness of the environmental light gradient was intermediate and dispersal distance of offspring was relatively small. In addition, our results predict that mutations that cause large shifts in the wavelength of peak absorption promote speciation, whereas we did not observe speciation when peak absorption evolved by stepwise mutations with small effect.

Conclusion: The results suggest that speciation can occur where environmental gradients create divergent selection on sensory modalities that are used in mate choice. Evidence for such gradients exists from several animal groups, and from freshwater and marine fishes in particular. The probability of speciation in a continuous population under such conditions may then critically depend on the genetic architecture of perceptual adaptation and female mate choice.

Show MeSH

Related in: MedlinePlus

The effects of environmental gradient and dispersal distance (a) and the effect of the size of mating area (b), carrying capacity (c), the size (horizontal extension) of habitat [x axis] (d), the relative strength of female preference (e), mutation mode, and mutation rate (f) on probability of speciation on probabilities of speciation. G = 0.10 and d = 50 except (a), M = 100 except (b), K = 10 except (c), habitat size = 1000 × 1000 except (d), α = 8 except (e), μ = 0.00001 except and 5 sites mutation model except (d and f), Male nuptial color is controlled by 100 loci. a) M = 100; b) d = 50, G = 0.10, Each cell in (a) and each value in (b) is a mean of 10 replicate simulations. Parameter values used as background in exploration of individual parameter space are highlighted (open circle).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC1941727&req=5

Figure 2: The effects of environmental gradient and dispersal distance (a) and the effect of the size of mating area (b), carrying capacity (c), the size (horizontal extension) of habitat [x axis] (d), the relative strength of female preference (e), mutation mode, and mutation rate (f) on probability of speciation on probabilities of speciation. G = 0.10 and d = 50 except (a), M = 100 except (b), K = 10 except (c), habitat size = 1000 × 1000 except (d), α = 8 except (e), μ = 0.00001 except and 5 sites mutation model except (d and f), Male nuptial color is controlled by 100 loci. a) M = 100; b) d = 50, G = 0.10, Each cell in (a) and each value in (b) is a mean of 10 replicate simulations. Parameter values used as background in exploration of individual parameter space are highlighted (open circle).

Mentions: For exploration of parameter space permissive of speciation, we modified each parameter, starting from a combination of parameters in which speciation was frequently observed (see Table 1 for the definitions of parameters): habitat size (x axis) = 1000, K (carrying capacity) = 10, d (the standard deviation of dispersal distance) = 50, M (mating area) = 100, GE (the steepness of the gradient in predominant light color) = 0.10, μ (mutation rates for all loci = 0.00001, 5 sites mutation model for opsin genes (see Mutation model senction in Methods), k (the relative contribution by an opsin gene to overall sensitivity, e.g. through differential expression of opsin genes) controlled by 10 additive loci, α (the strength of female preference relative to perception intensity) = 8, male nuptial color controlled by 100 additive loci. Fig. 2a reports the probabilities of speciation for different combinations of the steepness of the environmental gradient of predominant light color (ambient peak wavelength), (GE) and the dispersal distance of offspring (d). Speciation occurred most frequently when dispersal distance was small (standard deviation of dispersal distance 5–15% of the length of the environmental gradient) and GE was intermediate (GE = 0.10–0.15). Similar to dispersal distance, increasing the mating area (M) decreased the probability of speciation although the speciation probability for the smallest mating area modeled (M = 75 = 7.5% of the length of the environmental gradient) was smaller than those for M = 100 and 125 (Fig. 2b). With mating areas of a diameter of 22.5% and more of the length of the environmental gradient, no speciation was observed. Similarly, speciation became rare when the standard deviation of dispersal distance exceeded 22.5% of the length of the environmental gradient (Fig. 2a). Hence, within the above detailed parameter set, frequent speciation required that standard deviation of dispersal distance and diameter of the mating area do not exceed 22% of the length of the environmental gradient.


A genetically explicit model of speciation by sensory drive within a continuous population in aquatic environments.

Kawata M, Shoji A, Kawamura S, Seehausen O - BMC Evol. Biol. (2007)

The effects of environmental gradient and dispersal distance (a) and the effect of the size of mating area (b), carrying capacity (c), the size (horizontal extension) of habitat [x axis] (d), the relative strength of female preference (e), mutation mode, and mutation rate (f) on probability of speciation on probabilities of speciation. G = 0.10 and d = 50 except (a), M = 100 except (b), K = 10 except (c), habitat size = 1000 × 1000 except (d), α = 8 except (e), μ = 0.00001 except and 5 sites mutation model except (d and f), Male nuptial color is controlled by 100 loci. a) M = 100; b) d = 50, G = 0.10, Each cell in (a) and each value in (b) is a mean of 10 replicate simulations. Parameter values used as background in exploration of individual parameter space are highlighted (open circle).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1941727&req=5

Figure 2: The effects of environmental gradient and dispersal distance (a) and the effect of the size of mating area (b), carrying capacity (c), the size (horizontal extension) of habitat [x axis] (d), the relative strength of female preference (e), mutation mode, and mutation rate (f) on probability of speciation on probabilities of speciation. G = 0.10 and d = 50 except (a), M = 100 except (b), K = 10 except (c), habitat size = 1000 × 1000 except (d), α = 8 except (e), μ = 0.00001 except and 5 sites mutation model except (d and f), Male nuptial color is controlled by 100 loci. a) M = 100; b) d = 50, G = 0.10, Each cell in (a) and each value in (b) is a mean of 10 replicate simulations. Parameter values used as background in exploration of individual parameter space are highlighted (open circle).
Mentions: For exploration of parameter space permissive of speciation, we modified each parameter, starting from a combination of parameters in which speciation was frequently observed (see Table 1 for the definitions of parameters): habitat size (x axis) = 1000, K (carrying capacity) = 10, d (the standard deviation of dispersal distance) = 50, M (mating area) = 100, GE (the steepness of the gradient in predominant light color) = 0.10, μ (mutation rates for all loci = 0.00001, 5 sites mutation model for opsin genes (see Mutation model senction in Methods), k (the relative contribution by an opsin gene to overall sensitivity, e.g. through differential expression of opsin genes) controlled by 10 additive loci, α (the strength of female preference relative to perception intensity) = 8, male nuptial color controlled by 100 additive loci. Fig. 2a reports the probabilities of speciation for different combinations of the steepness of the environmental gradient of predominant light color (ambient peak wavelength), (GE) and the dispersal distance of offspring (d). Speciation occurred most frequently when dispersal distance was small (standard deviation of dispersal distance 5–15% of the length of the environmental gradient) and GE was intermediate (GE = 0.10–0.15). Similar to dispersal distance, increasing the mating area (M) decreased the probability of speciation although the speciation probability for the smallest mating area modeled (M = 75 = 7.5% of the length of the environmental gradient) was smaller than those for M = 100 and 125 (Fig. 2b). With mating areas of a diameter of 22.5% and more of the length of the environmental gradient, no speciation was observed. Similarly, speciation became rare when the standard deviation of dispersal distance exceeded 22.5% of the length of the environmental gradient (Fig. 2a). Hence, within the above detailed parameter set, frequent speciation required that standard deviation of dispersal distance and diameter of the mating area do not exceed 22% of the length of the environmental gradient.

Bottom Line: In addition, our results predict that mutations that cause large shifts in the wavelength of peak absorption promote speciation, whereas we did not observe speciation when peak absorption evolved by stepwise mutations with small effect.The results suggest that speciation can occur where environmental gradients create divergent selection on sensory modalities that are used in mate choice.Evidence for such gradients exists from several animal groups, and from freshwater and marine fishes in particular.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Graduate School of Sciences, Tohoku University, Sendai, Japan. kawata@mail.tains.tohoku.ac.jp

ABSTRACT

Background: The sensory drive hypothesis predicts that divergent sensory adaptation in different habitats may lead to premating isolation upon secondary contact of populations. Speciation by sensory drive has traditionally been treated as a special case of speciation as a byproduct of adaptation to divergent environments in geographically isolated populations. However, if habitats are heterogeneous, local adaptation in the sensory systems may cause the emergence of reproductively isolated species from a single unstructured population. In polychromatic fishes, visual sensitivity might become adapted to local ambient light regimes and the sensitivity might influence female preferences for male nuptial color. In this paper, we investigate the possibility of speciation by sensory drive as a byproduct of divergent visual adaptation within a single initially unstructured population. We use models based on explicit genetic mechanisms for color vision and nuptial coloration.

Results: We show that in simulations in which the adaptive evolution of visual pigments and color perception are explicitly modeled, sensory drive can promote speciation along a short selection gradient within a continuous habitat and population. We assumed that color perception evolves to adapt to the modal light environment that individuals experience and that females prefer to mate with males whose nuptial color they are most sensitive to. In our simulations color perception depends on the absorption spectra of an individual's visual pigments. Speciation occurred most frequently when the steepness of the environmental light gradient was intermediate and dispersal distance of offspring was relatively small. In addition, our results predict that mutations that cause large shifts in the wavelength of peak absorption promote speciation, whereas we did not observe speciation when peak absorption evolved by stepwise mutations with small effect.

Conclusion: The results suggest that speciation can occur where environmental gradients create divergent selection on sensory modalities that are used in mate choice. Evidence for such gradients exists from several animal groups, and from freshwater and marine fishes in particular. The probability of speciation in a continuous population under such conditions may then critically depend on the genetic architecture of perceptual adaptation and female mate choice.

Show MeSH
Related in: MedlinePlus