Predator-induced transgenerational plasticity of parental care behaviour in male three-spined stickleback fish across two generations.

Parental care is a critical determinant of offspring fitness, and parents adjust their care in response to ecological challenges, including predation risk. The experiences of both mothers and fathers can influence phenotypes of future generations (transgenerational plasticity). If it is adaptive for parents to alter parental care in response to predation risk, then we expect F1 and F2 offspring who receive transgenerational cues of predation risk to shift their parental care behaviour if these ancestral cues reliably predict a similarly risky environment as their F0 parents. Here, we used three-spined sticklebacks (Gasterosteus aculeatus) to understand how paternal exposure to predation risk prior to mating alters reproductive traits and parental care behaviour in unexposed F1 sons and F2 grandsons. Sons of predator-exposed fathers took more attempts to mate than sons of control fathers. F1 sons and F2 grandsons with two (maternal and paternal) predator-exposed grandfathers shifted their paternal care (fanning) behaviour in strikingly similar ways: they fanned less initially, but fanned more near egg hatching. This shift in fanning behaviour matches shifts observed in response to direct exposure to predation risk, suggesting a highly conserved response to pre-fertilization predator exposure that persists from the F0 to the F1 and F2 generations.

Repeated parallel differentiation of social learning differences in benthic and limnetic threespine stickleback fish.

Individuals can reduce sampling costs and increase foraging efficiency by using information provided by others. One simple form of social information use is delayed local enhancement or increased interest in a location because of the past presence of others. We tested for delayed local enhancement in two ecomorphs of stickleback fish, benthic and limnetic, from three different lakes with putative independent evolutionary origins. Two of these lakes have reproductively isolated ecomorphs (species-pairs), whereas in the third, a previously intact species-pair recently collapsed into a hybrid swarm. Benthic fish in both intact species-pair lakes were more likely to exhibit delayed local enhancement despite being more solitary than limnetic fish. Their behaviour and morphology suggest their current perceived risk and past evolutionary pressure from predation did not drive this difference. In the hybrid swarm lake, we found a reversal in patterns of social information use, with limnetic-looking fish showing delayed local enhancement rather than benthic-looking fish. Together, our results strongly support parallel differentiation of social learning differences in recently evolved fish species, although hybridization can apparently erode and possibly even reverse these differences.

Landscape transcriptomics as a tool for addressing global change effects across diverse species.

Landscape transcriptomics is an emerging field studying how genome-wide expression patterns reflect dynamic landscape-scale environmental drivers, including habitat, weather, climate, and contaminants, and the subsequent effects on organismal function. This field is benefitting from advancing and increasingly accessible molecular technologies, which in turn are allowing the necessary characterization of transcriptomes from wild individuals distributed across natural landscapes. This research is especially important given the rapid pace of anthropogenic environmental change and potential impacts that span levels of biological organization. We discuss three major themes in landscape transcriptomic research: connecting transcriptome variation across landscapes to environmental variation, generating and testing hypotheses about the mechanisms and evolution of transcriptomic responses to the environment, and applying this knowledge to species conservation and management. We discuss challenges associated with this approach and suggest potential solutions. We conclude that landscape transcriptomics has great promise for addressing fundamental questions in organismal biology, ecology, and evolution, while providing tools needed for conservation and management of species.

Sensory environment affects Icelandic threespine stickleback's anti-predator escape behaviour.

Human-induced changes in climate and habitats push populations to adapt to novel environments, including new sensory conditions, such as reduced visibility. We studied how colonizing newly formed glacial lakes with turbidity-induced low-visibility affects anti-predator behaviour in Icelandic threespine sticklebacks. We tested nearly 400 fish from 15 populations and four habitat types varying in visibility and colonization history in their reaction to two predator cues (mechano-visual versus olfactory) in high versus low-visibility light treatments. Fish reacted differently to the cues and were affected by lighting environment, confirming that cue modality and light levels are important for predator detection and evasion. Fish from spring-fed lakes, especially from the highlands (likely more diverged from marine fish than lowland fish), reacted fastest to mechano-visual cues and were generally most active. Highland glacial fish showed strong responses to olfactory cues and, counter to predictions from the flexible stem hypothesis, the greatest plasticity in response to light levels. This study, leveraging natural, repeated invasions of novel sensory habitats, (i) illustrates rapid changes in anti-predator behaviour that follow due to adaptation, early life experience, or both, and (ii) suggests an additional role for behavioural plasticity enabling population persistence in the face of frequent changes in environmental conditions.

Behavior-related gene regulatory networks: A new level of organization in the brain.

Neuronal networks are the standard heuristic model today for describing brain activity associated with animal behavior. Recent studies have revealed an extensive role for a completely distinct layer of networked activities in the brain-the gene regulatory network (GRN)-that orchestrates expression levels of hundreds to thousands of genes in a behavior-related manner. We examine emerging insights into the relationships between these two types of networks and discuss their interplay in spatial as well as temporal dimensions, across multiple scales of organization. We discuss properties expected of behavior-related GRNs by drawing inspiration from the rich literature on GRNs related to animal development, comparing and contrasting these two broad classes of GRNs as they relate to their respective phenotypic manifestations. Developmental GRNs also represent a third layer of network biology, playing out over a third timescale, which is believed to play a crucial mediatory role between neuronal networks and behavioral GRNs. We end with a special emphasis on social behavior, discuss whether unique GRN organization and cis-regulatory architecture underlies this special class of behavior, and review literature that suggests an affirmative answer.

Correction to 'Parenting behaviour is highly heritable in male stickleback'.

[This corrects the article DOI: 10.1098/rsos.171029.].

Sex differences in cognition and their relationship to male mate choice.

Male cognition has gained recognition as an important potential player in sexual selection. A number of studies have found positive correlations between male sexual signals and cognitive performance and/or female preferences for males with better cognitive performance, although other studies have not found these relationships. Sex roles can differ dramatically, and sex differences in selection on cognition likely follow from the different tasks associated with these sex roles. Here, using threespine stickleback Gasterosteus aculeatus, a species with clearly divergent sex roles and mutual mate choice, we focus on the cognitive trait inhibitory control because males must differentially respond to reproductive females versus other sticklebacks while defending territories and refrain from eating eggs and fry while performing paternal care. We presented fish with a detour task four times over a period of 7 days, allowing us to assess initial inhibitory control and improvement over time. We ask 1) whether there are sex differences in inhibitory control and 2) whether male mate choice is associated with female inhibitory control. Although males outperformed females on three different measures of detour task performance across four trials, these differences were largely explained by males being less neophobic than females. Females took more trials to successfully solve the detour task, even after accounting for sex differences in neophobia. Female cognitive abilities, however, were unrelated to the vigor with which males courted them. The equivocal results regarding sex differences in cognitive ability suggest further study given the very different selection pressures each sex experiences.

Brain differences in ecologically differentiated sticklebacks.

Populations that have recently diverged offer a powerful model for studying evolution. Ecological differences are expected to generate divergent selection on multiple traits, including neurobiological ones. Animals must detect, process, and act on information from their surroundings and the form of this information can be highly dependent on the environment. We might expect different environments to generate divergent selection not only on the sensory organs, but also on the brain regions responsible for processing sensory information. Here, we test this hypothesis using recently evolved reproductively isolated species pairs of threespine stickleback fish Gasterosteus aculeatus that have well-described differences in many morphological and behavioral traits correlating with ecological differences. We use a state-of-the-art method, magnetic resonance imaging, to get accurate volumetric data for 2 sensory processing regions, the olfactory bulbs and optic tecta. We found a tight correlation between ecology and the size of these brain regions relative to total brain size in 2 lakes with intact species pairs. Limnetic fish, which rely heavily on vision, had relatively larger optic tecta and smaller olfactory bulbs compared with benthic fish, which utilize olfaction to a greater extent. Benthic fish also had larger total brain volumes relative to their body size compared with limnetic fish. These differences were erased in a collapsed species pair in Enos Lake where anthropogenic disturbance has led to intense hybridization. Together these data indicate that evolution of sensory processing regions can occur rapidly and independently.

Why does the magnitude of genotype-by-environment interaction vary?

Genotype-by-environment interaction (G × E), that is, genetic variation in phenotypic plasticity, is a central concept in ecology and evolutionary biology. G×E has wide-ranging implications for trait development and for understanding how organisms will respond to environmental change. Although G × E has been extensively documented, its presence and magnitude vary dramatically across populations and traits. Despite this, we still know little about why G × E is so evident in some traits and populations, but minimal or absent in others. To encourage synthetic research in this area, we review diverse hypotheses for the underlying biological causes of variation in G × E. We extract common themes from these hypotheses to develop a more synthetic understanding of variation in G × E and suggest some important next steps.

Parenting behaviour is highly heritable in male stickleback.

Parental care is critical for fitness, yet little is known about its genetic basis. Here, we estimate the heritability of parenting behaviour in a species famous for its diversity and its behavioural repertoire: three-spined stickleback (Gasterosteus aculeatus). Male three-spined stickleback are the sole providers of parental care that is necessary for offspring survival; therefore, this system offers the opportunity to study the inheritance of parental behaviour when selection is primarily acting on males. Fanning behaviour is a conspicuous parental behaviour that is readily quantified in this species. We show that the heritability of fanning behaviour is ≥0.9 and significantly different from zero within a freshwater population. Moreover, there was abundant genetic variation for fanning behaviour, indicating that it could readily evolve. These results suggest that parenting behaviour is tractable for further genetic dissection in this system.

The relationship between male sexual signals, cognitive performance, and mating success in stickleback fish.

Cognitive ability varies dramatically among individuals, yet the manner in which this variation correlates with reproduction has rarely been investigated. Here, we ask (1) do male sexual signals reflect their cognitive ability, and (2) is cognitive ability associated with male mating success? Specifically, we presented threespine sticklebacks (Gasterosteus aculeatus) with a detour-reaching task to assess initial inhibitory control. Fish that performed better were those who solved the detour-reaching task, solved it faster, and required fewer attempts to solve. We then reexamined males' performance on this task over several days to assess learning ability in this context. We next measured sexual signals (coloration, nest area, and courtship vigor) and asked whether they reveal information about these male cognitive abilities. Finally, we examined whether success at attracting a female is associated with male cognition. After controlling for the strong effect of neophobia, we found that no measured sexual signals were associated with initial inhibitory control. Sexual signals were also not associated with change in performance on the detour-reaching task over time (learning). However, females preferred mating with males who had better initial inhibitory control. We speculate that inhibitory control is a critical trait for male sticklebacks. In this system, males perform all parental care, but must avoid eating their own fry which closely resemble their prey items. Therefore, males with better inhibitory control may be more likely to successfully raise their offspring to independence. Our research adds to a growing list of mating systems and taxa in which cognition is important for measures related to fitness.

Male competition fitness landscapes predict both forward and reverse speciation.

Speciation is facilitated when selection generates a rugged fitness landscape such that populations occupy different peaks separated by valleys. Competition for food resources is a strong ecological force that can generate such divergent selection. However, it is unclear whether intrasexual competition over resources that provide mating opportunities can generate rugged fitness landscapes that foster speciation. Here we use highly variable male F2 hybrids of benthic and limnetic threespine sticklebacks, Gasterosteus aculeatus Linnaeus, 1758, to quantify the male competition fitness landscape. We find that disruptive sexual selection generates two fitness peaks corresponding closely to the male phenotypes of the two parental species, favouring divergence. Most surprisingly, an additional region of high fitness favours novel hybrid phenotypes that correspond to those observed in a recent case of reverse speciation after anthropogenic disturbance. Our results reveal that sexual selection through male competition plays an integral role in both forward and reverse speciation.

Comment on "Illusions promote mating success in great bowerbirds".

Kelley and Endler (Reports, 20 January 2012, p. 335) claim that male great bowerbirds construct a visual illusion, using display object gradients, that affects mating success. We argue that they provide inadequate statistical support for their hypothesis, inappropriately exclude important data, and do not consider other display traits that explain mating success. We propose a more plausible alternative hypothesis to explain display object patterns.

Aerobic capacity in wild satin bowerbirds: repeatability and effects of age, sex and condition.

Individual variation in aerobic capacity has been extensively studied, especially with respect to condition, maturity or pathogen infection, and to gain insights into mechanistic foundations of performance. However, its relationship to mate competition is less well understood, particularly for animals in natural habitats. We examined aerobic capacity [maximum rate of O2 consumption (VO2,max) in forced exercise] in wild satin bowerbirds, an Australian passerine with a non-resource based mating system and strong intermale sexual competition. We tested for repeatability of mass and VO2,max, differences among age and sex classes, and effects of several condition indices. In adult males, we examined interactions between aerobic performance and bower ownership (required for male mating success). There was significant repeatability of mass and VO2,max within and between years, but between-year repeatability was lower than within-year repeatability. VO2,max varied with an overall scaling to mass(0.791), but most variance in VO2,max was not explained by mass. Indicators of condition (tarsus and wing length asymmetry, the ratio of tarsus length to mass) were not correlated to VO2,max. Ectoparasite counts were weakly correlated to VO2,max across all age-sex classes but not within any class. Adult males, the cohort with the most intense levels of mating competition, had higher VO2,max than juvenile birds or adult females. However, there was no difference between the VO2,max of bower-owning males and that of males not known to hold bowers. Thus one major factor determining male reproductive success was not correlated to aerobic performance.