Can behaviour impede evolution? Persistence of singing effort after morphological song loss in crickets

Evolutionary loss of sexual signals is widespread. Examining the consequences for behaviours associated with such signals can provide insight into factors promoting or inhibiting trait loss. We tested whether a behavioural component of a sexual trait, male calling effort, has been evolutionary reduced in silent populations of Hawaiian field crickets ( Teleogryllus oceanicus ) . Cricket song requires energetically costly wing movements, but ‘flatwing’ males have feminized wings that preclude song and protect against a lethal, eavesdropping parasitoid. Flatwing males express wing movement patterns associated with singing but, in contrast with normal-wing males, sustained periods of wing movement cannot confer sexual selection benefits and should be subject to strong negative selection. We developed an automated technique to quantify how long males spend expressing wing movements associated with song. We compared calling effort among populations of Hawaiian crickets with differing proportions of silent males and between male morphs. Contrary to expectation, silent populations invested as much in calling effort as non-silent populations. Additionally, flatwing and normal-wing males from the same population did not differ in calling effort. The lack of evolved behavioural adjustment following morphological change in silent Hawaiian crickets illustrates how behaviour might sometimes impede, rather than facilitate, evolution.

Parallel genomic architecture underlies repeated sexual signal divergence in Hawaiian Laupala crickets

When the same phenotype evolves repeatedly, we can explore the predictability of genetic changes underlying phenotypic evolution. Theory suggests that genetic parallelism is less likely when phenotypic changes are governed by many small-effect loci compared to few of major effect, because different combinations of genetic changes can result in the same quantitative outcome. However, some genetic trajectories might be favoured over others, making a shared genetic basis to repeated polygenic evolution more likely. To examine this, we studied the genetics of parallel male mating song evolution in the Hawaiian cricket Laupala . We compared quantitative trait loci (QTL) underlying song divergence in three species pairs varying in phenotypic distance. We tested whether replicated song divergence between species involves the same QTL and whether the likelihood of QTL sharing is related to QTL effect size. Contrary to theoretical predictions, we find substantial parallelism in polygenic genetic architectures underlying repeated song divergence. QTL overlapped more frequently than expected based on simulated QTL analyses. Interestingly, QTL effect size did not predict QTL sharing, but did correlate with magnitude of phenotypic divergence. We highlight potential mechanisms driving these constraints on cricket song evolution and discuss a scenario that consolidates empirical quantitative genetic observations with micro-mutational theory.

Parallel genomic architecture underlies repeated sexual signal divergence in Hawaiian Laupala crickets

ABSTRACTWhen the same phenotype evolves repeatedly, we can explore the predictability of genetic changes underlying phenotypic evolution. Theory suggests that genetic parallelism is less likely when phenotypic changes are governed by many small-effect loci compared to few of major effect, because different combinations of genetic changes can result in the same quantitative outcome. However, some genetic trajectories might be favored over others, making a shared genetic basis to repeated polygenic evolution more likely. To examine this, we studied the genetics of parallel male mating song evolution in the Hawaiian cricket Laupala. We compared quantitative trait loci (QTL) underlying song divergence in three species pairs varying in phenotypic distance. We tested whether replicated song divergence between species involves the same QTL and the likelihood that sharing QTL is related to phenotypic effect sizes. Contrary to theoretical predictions, we find substantial parallelism in polygenic genetic architectures underlying repeated song divergence. QTL overlapped more than expected based on simulated QTL analyses. Interestingly, QTL effect size did not predict QTL sharing, but did correlate with magnitude of phenotypic divergence. We highlight potential mechanisms driving these constraints on cricket song evolution and discuss a scenario that consolidates empirical quantitative genetic observations with micro-mutational theory.

Guide to Crickets of Australia

Cricket song is a sound of the Australian bush. Even in cities, the rasping calls signify Australia’s remarkable cricket biodiversity. Crickets are notable for a variety of reasons. When their population booms, some of these species become agricultural pests and destroy crop pastures. Some introduced species are of biosecurity concern. Other crickets are important food sources for native birds, reptiles and mammals, as well as domestic pets. Soon you might even put them in your cake or stir-fry, as there is a rapidly growing industry for cricket products for human consumption. Featuring keys, distribution maps, illustrations and detailed colour photographs from CSIRO’s Australian National Insect Collection, A Guide to Crickets of Australia allows readers to reliably identify all 92 described genera and many species from the Grylloidea (true crickets) and Gryllotalpoidea (mole crickets and ant crickets) superfamilies. Not included are the Raspy Crickets (Gryllacrididae), King Crickets (Anostostomatidae) or the so-called ‘Pygmy Mole Crickets’ (Caelifera), which despite their common names are not related to true crickets. Natural history enthusiasts and professionals will find this an essential guide.

The genetics of behavioral isolation in an island system

Mating behavior divergence can make significant contributions to reproductive isolation and speciation in various biogeographic contexts. However, whether the genetic architecture underlying mating behavior divergence is related to the biogeographic history and the tempo and mode of speciation remains poorly understood. Here, we use quantitative trait locus (QTL) mapping to infer the number, distribution, and effect size of mating song rhythm variation in the crickets Laupala eukolea and L. cerasina, which occur on different islands (Maui and Hawai’i). We then compare these results with a similar study of an independently evolving species pair that diverged within the same island. Finally, we annotate the L. cerasina transcriptome and test whether QTL fall in functionally enriched genomic regions. We document a polygenic architecture behind song rhythm divergence in the inter-island species pair that is remarkably similar to that previously found for an intra-island species pair in the same genus. Importantly, QTL regions were significantly enriched for potential homologs of genes involved in pathways that may be modulating cricket song rhythm. These clusters of loci could constrain the spatial genomic distribution of genetic variation underlying cricket song variation and harbor several candidate genes that merit further study.

Stay tuned: active amplification tunes tree-cricket ears to track temperature-dependent song frequency

Tree cricket males produce tonal songs, used for mate-attraction and male-male interactions. Active mechanics tunes hearing to conspecific song frequency. However, tree cricket song frequency increases with temperature, presenting a problem for tuned listeners. We show that the actively amplified frequency increases with temperature, thus shifting mechanical and neuronal auditory tuning to maintain a match with conspecific song frequency. Active auditory processes are known from several taxa, but their adaptive function has rarely been demonstrated. We show that tree crickets harness active processes to ensure that auditory tuning remains matched to conspecific song frequency, despite changing environmental conditions and signal characteristics. Adaptive tuning allows tree crickets to selectively detect potential mates or rivals over large distances and is likely to bestow a strong selective advantage by reducing mate-finding effort and facilitating intermale interactions.

Stay tuned: active amplification tunes tree cricket ears to track temperature-dependent song frequency

Tree cricket males produce tonal songs, used for mate attraction and male–male interactions. Active mechanics tunes hearing to conspecific song frequency. However, tree cricket song frequency increases with temperature, presenting a problem for tuned listeners. We show that the actively amplified frequency increases with temperature, thus shifting mechanical and neuronal auditory tuning to maintain a match with conspecific song frequency. Active auditory processes are known from several taxa, but their adaptive function has rarely been demonstrated. We show that tree crickets harness active processes to ensure that auditory tuning remains matched to conspecific song frequency, despite changing environmental conditions and signal characteristics. Adaptive tuning allows tree crickets to selectively detect potential mates or rivals over large distances and is likely to bestow a strong selective advantage by reducing mate-finding effort and facilitating intermale interactions.

Dynamics of Cricket Sound Production

The clever designs of natural transducers are a great source of inspiration for man-made systems. At small length scales, there are many transducers in nature that we are now beginning to understand and learn from. Here, we present an example of such a transducer that is used by field crickets to produce their characteristic song. This transducer uses two distinct components—a file of discrete teeth and a plectrum that engages intermittently to produce a series of impulses forming the loading, and an approximately triangular membrane, called the harp, that acts as a resonator and vibrates in response to the impulse-train loading. The file-and-plectrum act as a frequency multiplier taking the low wing beat frequency as the input and converting it into an impulse-train of sufficiently high frequency close to the resonant frequency of the harp. The forced vibration response results in beats producing the characteristic sound of the cricket song. With careful measurements of the harp geometry and experimental measurements of its mechanical properties (Young's modulus determined from nanoindentation tests), we construct a finite element (FE) model of the harp and carry out modal analysis to determine its natural frequency. We fine tune the model with appropriate elastic boundary conditions to match the natural frequency of the harp of a particular species—Gryllus bimaculatus. We model impulsive loading based on a loading scheme reported in literature and predict the transient response of the harp. We show that the harp indeed produces beats and its frequency content matches closely that of the recorded song. Subsequently, we use our FE model to show that the natural design is quite robust to perturbations in the file. The characteristic song frequency produced is unaffected by variations in the spacing of file-teeth and even by larger gaps. Based on the understanding of how this natural transducer works, one can design and fabricate efficient microscale acoustic devices such as microelectromechanical systems (MEMS) loudspeakers.