Limits...
Female mate choice can drive the evolution of high frequency echolocation in bats: a case study with Rhinolophus mehelyi.

Puechmaille SJ, Borissov IM, Zsebok S, Allegrini B, Hizem M, Kuenzel S, Schuchmann M, Teeling EC, Siemers BM - PLoS ONE (2014)

Bottom Line: Natural selection favours signals, receptors, and signalling behaviour that optimise the received signal relative to background noise.Sexual selection through mate choice can strongly modify the effects of natural selection on signalling systems ultimately causing maladaptive signals to evolve.Our data refute the sole role of ecology in the evolution of echolocation and highlight the antagonistic interplay between natural and sexual selection in shaping acoustic signals.

View Article: PubMed Central - PubMed

Affiliation: Sensory Ecology Group, Max Planck Institute for Ornithology, Seewiesen, Germany; School of Biology & Environmental Science, University College Dublin, Belfield, Dublin, Ireland; Tabachka Bat Research Station, Tabachka, Bulgaria.

ABSTRACT
Animals employ an array of signals (i.e. visual, acoustic, olfactory) for communication. Natural selection favours signals, receptors, and signalling behaviour that optimise the received signal relative to background noise. When the signal is used for more than one function, antagonisms amongst the different signalling functions may constrain the optimisation of the signal for any one function. Sexual selection through mate choice can strongly modify the effects of natural selection on signalling systems ultimately causing maladaptive signals to evolve. Echolocating bats represent a fascinating group in which to study the evolution of signalling systems as unlike bird songs or frog calls, echolocation has a dual role in foraging and communication. The function of bat echolocation is to generate echoes that the calling bat uses for orientation and food detection with call characteristics being directly related to the exploitation of particular ecological niches. Therefore, it is commonly assumed that echolocation has been shaped by ecology via natural selection. Here we demonstrate for the first time using a novel combined behavioural, ecological and genetic approach that in a bat species, Rhinolophus mehelyi: (1) echolocation peak frequency is an honest signal of body size; (2) females preferentially select males with high frequency calls during the mating season; (3) high frequency males sire more off-spring, providing evidence that echolocation calls may play a role in female mate choice. Our data refute the sole role of ecology in the evolution of echolocation and highlight the antagonistic interplay between natural and sexual selection in shaping acoustic signals.

Show MeSH

Related in: MedlinePlus

Correlation between an individual’s peak frequency and average relatedness with other members of the colony.Data are presented for (A), females (n = 29) and (B), males (n = 28) of El Haouariya colony (see text for statistical results). The solid back line represents a linear regression between peak frequency and relatedness and the dashed lines the 95% confidence interval of this regression.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4116191&req=5

pone-0103452-g004: Correlation between an individual’s peak frequency and average relatedness with other members of the colony.Data are presented for (A), females (n = 29) and (B), males (n = 28) of El Haouariya colony (see text for statistical results). The solid back line represents a linear regression between peak frequency and relatedness and the dashed lines the 95% confidence interval of this regression.

Mentions: To provide further data supporting that females indeed choose their mate according to peak frequency and specifically prefer males with high frequency, we investigated the relationship between a proxy of reproductive success (mean relatedness) and peak frequency. No significant relationship was found between the two variables in the R. mehelyi colony of Zorovitza (females, n = 57, rho  = 0.03, P = 0.48; males, n = 36, rho  = 0.05, P = 0.38) but this result was expected given the very low power of the test as only 2–3% of this large colony of circa 4000–5000 animals were sampled. To increase the power of the test, we therefore applied the same analysis to a smaller colony of circa 300 animals (El Haouariya colony) where circa 20% of the colony was sampled with similar number of males and females. As expected if echolocation frequency is playing a role in mate choice, we found no significant relationship between mean relatedness between colony members and peak frequency for adult females (n = 29, rho = 0.06, P = 0.38; Figure 4A) but we did find a strong and significant relationship for adult males (n = 28, rho = 0.47, P = 0.005; Figure 4B). This significant positive relationship in adult males was also obtained using three other relatedness estimates (Lynch & Li, Triadic and Dyadic likelihood; Spearman rank correlation test, n = 28, rho = 0.55, 0.41 & 0.31, P = 0.001, 0.015 & 0.05 respectively). In support of ongoing directional sexual selection for high call frequencies, we found that the distribution of echolocation frequencies was not normally distributed in adult individuals of the species (Shapiro-Wilk test, P<0.001) but was left-skewed (D’Agostino skewness test, P = 0.028).


Female mate choice can drive the evolution of high frequency echolocation in bats: a case study with Rhinolophus mehelyi.

Puechmaille SJ, Borissov IM, Zsebok S, Allegrini B, Hizem M, Kuenzel S, Schuchmann M, Teeling EC, Siemers BM - PLoS ONE (2014)

Correlation between an individual’s peak frequency and average relatedness with other members of the colony.Data are presented for (A), females (n = 29) and (B), males (n = 28) of El Haouariya colony (see text for statistical results). The solid back line represents a linear regression between peak frequency and relatedness and the dashed lines the 95% confidence interval of this regression.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4116191&req=5

pone-0103452-g004: Correlation between an individual’s peak frequency and average relatedness with other members of the colony.Data are presented for (A), females (n = 29) and (B), males (n = 28) of El Haouariya colony (see text for statistical results). The solid back line represents a linear regression between peak frequency and relatedness and the dashed lines the 95% confidence interval of this regression.
Mentions: To provide further data supporting that females indeed choose their mate according to peak frequency and specifically prefer males with high frequency, we investigated the relationship between a proxy of reproductive success (mean relatedness) and peak frequency. No significant relationship was found between the two variables in the R. mehelyi colony of Zorovitza (females, n = 57, rho  = 0.03, P = 0.48; males, n = 36, rho  = 0.05, P = 0.38) but this result was expected given the very low power of the test as only 2–3% of this large colony of circa 4000–5000 animals were sampled. To increase the power of the test, we therefore applied the same analysis to a smaller colony of circa 300 animals (El Haouariya colony) where circa 20% of the colony was sampled with similar number of males and females. As expected if echolocation frequency is playing a role in mate choice, we found no significant relationship between mean relatedness between colony members and peak frequency for adult females (n = 29, rho = 0.06, P = 0.38; Figure 4A) but we did find a strong and significant relationship for adult males (n = 28, rho = 0.47, P = 0.005; Figure 4B). This significant positive relationship in adult males was also obtained using three other relatedness estimates (Lynch & Li, Triadic and Dyadic likelihood; Spearman rank correlation test, n = 28, rho = 0.55, 0.41 & 0.31, P = 0.001, 0.015 & 0.05 respectively). In support of ongoing directional sexual selection for high call frequencies, we found that the distribution of echolocation frequencies was not normally distributed in adult individuals of the species (Shapiro-Wilk test, P<0.001) but was left-skewed (D’Agostino skewness test, P = 0.028).

Bottom Line: Natural selection favours signals, receptors, and signalling behaviour that optimise the received signal relative to background noise.Sexual selection through mate choice can strongly modify the effects of natural selection on signalling systems ultimately causing maladaptive signals to evolve.Our data refute the sole role of ecology in the evolution of echolocation and highlight the antagonistic interplay between natural and sexual selection in shaping acoustic signals.

View Article: PubMed Central - PubMed

Affiliation: Sensory Ecology Group, Max Planck Institute for Ornithology, Seewiesen, Germany; School of Biology & Environmental Science, University College Dublin, Belfield, Dublin, Ireland; Tabachka Bat Research Station, Tabachka, Bulgaria.

ABSTRACT
Animals employ an array of signals (i.e. visual, acoustic, olfactory) for communication. Natural selection favours signals, receptors, and signalling behaviour that optimise the received signal relative to background noise. When the signal is used for more than one function, antagonisms amongst the different signalling functions may constrain the optimisation of the signal for any one function. Sexual selection through mate choice can strongly modify the effects of natural selection on signalling systems ultimately causing maladaptive signals to evolve. Echolocating bats represent a fascinating group in which to study the evolution of signalling systems as unlike bird songs or frog calls, echolocation has a dual role in foraging and communication. The function of bat echolocation is to generate echoes that the calling bat uses for orientation and food detection with call characteristics being directly related to the exploitation of particular ecological niches. Therefore, it is commonly assumed that echolocation has been shaped by ecology via natural selection. Here we demonstrate for the first time using a novel combined behavioural, ecological and genetic approach that in a bat species, Rhinolophus mehelyi: (1) echolocation peak frequency is an honest signal of body size; (2) females preferentially select males with high frequency calls during the mating season; (3) high frequency males sire more off-spring, providing evidence that echolocation calls may play a role in female mate choice. Our data refute the sole role of ecology in the evolution of echolocation and highlight the antagonistic interplay between natural and sexual selection in shaping acoustic signals.

Show MeSH
Related in: MedlinePlus