Measuring heritability: Why bother?

Uchiyama et al. rightly consider how cultural variation may influence estimates of heritability by contributing to environmental sources of variation. We disagree, however, with the idea that generalisable estimates of heritability are ever a plausible aim. Heritability estimates are always context-specific, and to suggest otherwise is to misunderstand what heritability can and cannot tell us.

Environmental Correlates of Sexual Signaling in the Heteroptera: A Prospective Study.

Sexual selection is a major evolutionary process, shaping organisms in terms of success in competition for access to mates and their gametes. The study of sexual selection has provided rich empirical and theoretical literature addressing the ecological and evolutionary causes and consequences of competition for gametes. However, there remains a bias towards individual, species-specific studies, whilst broader, cross-species comparisons looking for wider-ranging patterns in sexual selection remain uncommon. For instance, we are still some ways from understanding why particular kinds of traits tend to evolve under sexual selection, and under what circumstances. Here we consider sexual selection in the Heteroptera, a sub-order of the Hemiptera, or true bugs. The latter is the largest of the hemimetabolous insect orders, whilst the Heteroptera itself comprises some 40,000-plus described species. We focus on four key sexual signaling modes found in the Heteroptera: chemical signals, acoustic signaling via stridulation, vibrational (substrate) signaling, and finally tactile signaling (antennation). We compare how these modes vary across broad habitat types and provide a review of each type of signal. We ask how we might move towards a more predictive theory of sexual selection, that links mechanisms and targets of sexual selection to various ecologies.

The definition of sexual selection.

Sexual selection is a key component of evolutionary biology. However, from the very formulation of sexual selection by Darwin, the nature and extent of sexual selection have been controversial. Recently, such controversy has led back to the fundamental question of just what sexual selection is. This has included how we incorporate female-female reproductive competition into sexual or natural selection. In this review, we do four things. First, we examine what we want a definition to do. Second, we define sexual selection: sexual selection is any selection that arises from fitness differences associated with nonrandom success in the competition for access to gametes for fertilization. An important outcome of this is that as mates often also offer access to resources, when those resources are the targets of the competition, rather than their gametes, the process should be considered natural rather than sexual selection. We believe this definition encapsulates both much of Darwin's original thinking about sexual selection, and much of how contemporary biologists use the concept of sexual selection. Third, we address alternative definitions, focusing in some detail on the role of female reproductive competition. Fourth, we challenge our definition with a number of scenarios, for instance where natural and sexual selection may align (as in some forms of endurance rivalry), or where differential allocation means teasing apart how fecundity and access to gametes influence fitness. In conclusion, we emphasize that whilst the ecological realities of sexual selection are likely to be complex, the definition of sexual selection is rather simple.

Context-dependent use of visual cues in the shell selection behaviour of the hermit crab Pagurus bernhardus.

Animals avoid predator attack in different ways; some carry defensive structures to reduce predation, with the classic example being hermit crabs and their use of a mollusc shell as a portable refugium. During shell selection, various shell characteristics are investigated by the crab to determine their suitability. Here we consider the role of visual cues. Previous research suggests that some hermit crabs are more likely to initially choose a conspicuous shell but also to move to backgrounds against which they are less conspicuous, suggesting a short-term/long-term trade-off. Across experiments in which we manipulated shell and background colour, we show initially that Pagurus bernhardus prefer black shells over white but this preference was lost in the absence of visual cues. We then show that the strength of preference was dependent on background colour. We repeated this last experiment with red and yellow shells against red or yellow backgrounds to investigate whether this preference extended to chromatic hues. A preference for darker (red) shells was expressed, but preference alteration with background was not observed. P. bernhardus therefore discriminate between shells in terms of shell and background colour, and discrimination may be rooted in a preference for darker shaded shells.

The rationality of decisions depends on behavioural context.

Decision makers can be described as economically rational (making consistent choices), or economically irrational (making choices that vary with the options available). As the extent to which animals can and do make rational versus irrational decisions remains unclear, we tested the decision-making strategies of female Nasonia vitripennis parasitic wasps in two behavioural contexts: oviposition and foraging. In our first experiment, to determine whether oviposition preferences changed depending on the options available, we presented females with a high and a medium-quality blow fly host to parasitize, and gave some females an additional low or very low quality 'decoy' host. Presence of decoy options did not affect females' oviposition choices, either in willingness to parasitize a host or the number of offspring laid. In our second experiment, we tested the effects of a low-quality decoy option on foraging preference for a high and a medium-quality sucrose concentration option. Here, presence of the low-quality decoy enhanced female preference for the high-quality option. Females therefore made economically rational decisions when ovipositing and economically irrational decisions when foraging. This difference in decision outcomes suggests that the cost/benefit ratio of making one type of decision over another may differ with the behavioural task.

A single pleiotropic locus influences the rate of hybridization between two sibling species of Lygaeus bugs.

The evolution of reproductive isolation lies at the heart of understanding the process of speciation. Of particular interest is the relationship between pre- and postzygotic reproductive isolation, and the genetic architecture of traits that contribute to one or both forms of reproductive isolation. The sibling species of seed bug Lygaeus equestris and L. simulans show a classic pattern of asymmetric prezygotic reproductive isolation, with female L. equestris hybridizing with male L. simulans, but with no hybridization in the reciprocal direction. We have recently described a mutant pale color form of L. simulans, that inherits as a single Mendelian locus and is pleiotropic for a number of other life history and behavioral traits. Here, we tested whether this locus also influences pre- and postzygotic reproductive isolation. Two sets of experimental crosses revealed that behavioral isolation varied with mutant versus wild-type phenotype for male L. simulans, with the pale form less successful at mating with female L. equestris. In terms of trying to assess postzygotic isolation, levels of hybrid offspring production were uniformly low across the experiments. However, we did obtain, for the first time, hybrid offspring from a pairing between a female L. simulans and a male L. equestris. In this instance, the female was of the pale mutant genotype. Together with evidence for heterozygote advantage in terms of nymph survival, we consider our results in terms of possible mechanisms of reproductive isolation between this species pair, the role of the pale mutation, and the possible genetic architectures underlying the mutation, from a single gene to a supergene.

Same-sex sexual behaviour.

Balfour and Shuker introduce animal sexual behaviors directed to members of the same sex.

Genomics of sex allocation in the parasitoid wasp Nasonia vitripennis.

BACKGROUND: Whilst adaptive facultative sex allocation has been widely studied at the phenotypic level across a broad range of organisms, we still know remarkably little about its genetic architecture. Here, we explore the genome-wide basis of sex ratio variation in the parasitoid wasp Nasonia vitripennis, perhaps the best studied organism in terms of sex allocation, and well known for its response to local mate competition. RESULTS: We performed a genome-wide association study (GWAS) for single foundress sex ratios using iso-female lines derived from the recently developed outbred N. vitripennis laboratory strain HVRx. The iso-female lines capture a sample of the genetic variation in HVRx and we present them as the first iteration of the Nasonia vitripennis Genome Reference Panel (NVGRP 1.0). This panel provides an assessment of the standing genetic variation for sex ratio in the study population. Using the NVGRP, we discovered a cluster of 18 linked SNPs, encompassing 9 annotated loci associated with sex ratio variation. Furthermore, we found evidence that sex ratio has a shared genetic basis with clutch size on three different chromosomes. CONCLUSIONS: Our approach provides a thorough description of the quantitative genetic basis of sex ratio variation in Nasonia at the genome level and reveals a number of inter-related candidate loci underlying sex allocation regulation.

Validating the Demethylating Effects of 5-aza-2'-deoxycytidine in Insects Requires a Whole-Genome Approach.

We previously demonstrated that treatment with the demethylating agent 5-aza-2'-deoxycytidine (5-aza-dC) alters the offspring sex ratios produced by females of the parasitoid wasp Nasonia vitripennis. Females allocate offspring sex ratio in line with local mate competition theory, producing more or less female-biased sex ratios as the number of other females laying eggs on a patch varies, thereby reducing competition among their sons for mates. Interestingly, treatment with 5-aza-dC did not ablate the facultative sex allocation response. Instead, sex ratios became less female biased, a shift in the direction of the optimum sex ratio for paternally inherited alleles according to genomic conflict theory. This was the first (albeit indirect) experimental evidence for genomic conflict over sex allocation. In their comment, Ellers and colleagues assayed the effects of 5-aza-dC on DNA methylation in 10 Nasonia genes, finding no evidence of demethylation in these 10 genes, from which they conclude that 5-aza-dC has no demethylating capability in N. vitripennis. Quantifying the efficacy of 5-aza-dC in terms of demethylation is indeed crucial to in-depth interpretation of studies using 5-aza-dC to link phenotypes to epigenetic regulation. Here we outline the mode of action of 5-aza-dC and demonstrate that determining the efficacy of 5-aza-dC in insect systems requires a whole-genome approach.

Supergenes.

Daniella Black and David M. Shuker introduce supergenes - clusters of genes that control complex traits and are inherited together.

An Inconvenient Truth: The Unconsidered Benefits of Convenience Polyandry.

Polyandry, or multiple mating by females with different males, is commonplace. One explanation is that females engage in convenience polyandry, mating multiple times to reduce the costs of sexual harassment. Although the logic underlying convenience polyandry is clear, and harassment often seems to influence mating outcomes, it has not been subjected to as thorough theoretical or empirical attention as other explanations for polyandry. We re-examine here convenience polyandry in the light of new studies demonstrating previously unconsidered benefits of polyandry. We suggest that true convenience polyandry is likely to be a fleeting phenomenon, even though it can profoundly shape mating-system evolution via potential feedback loops between resistance to males and the costs and benefits of mating.

Cryptic male choice.

Cédric Aumont and David Shuker introduce cryptic male choice, the process by which males bias fertilization during copulation.

Differential gene expression is not required for facultative sex allocation: a transcriptome analysis of brain tissue in the parasitoid wasp Nasonia vitripennis.

Whole-transcriptome technologies have been widely used in behavioural genetics to identify genes associated with the performance of a behaviour and provide clues to its mechanistic basis. Here, we consider the genetic basis of sex allocation behaviour in the parasitoid wasp Nasonia vitripennis. Female Nasonia facultatively vary their offspring sex ratio in line with Hamilton's theory of local mate competition (LMC). A single female or 'foundress' laying eggs on a patch will lay just enough sons to fertilize her daughters. As the number of 'foundresses' laying eggs on a patch increases (and LMC declines), females produce increasingly male-biased sex ratios. Phenotypic studies have revealed the cues females use to estimate the level of LMC their sons will experience, but our understanding of the genetics underlying sex allocation is limited. Here, we exposed females to three foundress number conditions, i.e. three LMC conditions, and allowed them to oviposit. mRNA was extracted from only the heads of these females to target the brain tissue. The subsequent RNA-seq experiment confirmed that differential gene expression is not associated with the response to sex allocation cues and that we must instead turn to the underlying neuroscience to reveal the underpinnings of this impressive behavioural plasticity.

The fitness effects of a pale mutant in the aposematic seed bug Lygaeus simulans indicate pleiotropy between warning coloration and life history.

Conspicuous warning colors that signal chemical or other defenses are common in the natural world. For instance, such aposematic warning patterns of red-and-black or yellow-and-black are common among insect taxa, particularly in the order Hemiptera, often forming the basis of Batesian and/or Müllerian mimicry rings. In addition, it has been repeatedly noted that color polymorphisms or mutants that influence pigmentation can show pleiotropy with other behavioral, physiological, or life-history traits. Here, we describe a pale mutant of the seed bug Lygaeus simulans that appeared in our laboratory population in 2012, which differs in color to the wild-type bugs. Through multigenerational experimental crosses between wild-type and pale mutant L. simulans, we first show that the pale phenotype segregates as a single Mendelian locus, with the pale allele being recessive to the wild type. Next, we show (a) that there is a large heterozygous advantage in terms of fecundity, (b) that pale females suffer reduced longevity, and (c) that pale males have increased body length compared to wild-type homozygotes. Our data therefore suggest that the color locus is pleiotropic with a number of life-history traits, opening the door for a more complete genetic analysis of aposematic coloration in this species. In addition, this phenotype will be useful as a visible genetic marker, providing a tool for investigating sperm competition and other post-copulatory drivers of sexual selection in this species.

General intelligence does not help us understand cognitive evolution.

Burkart et al. conflate the domain-specificity of cognitive processes with the statistical pattern of variance in behavioural measures that partly reflect those processes. General intelligence is a statistical abstraction, not a cognitive trait, and we argue that the former does not warrant inferences about the nature or evolution of the latter.

Variation in pre- and post-copulatory sexual selection on male genital size in two species of lygaeid bug.

ABSTRACT: Sexual selection has been shown to be the driving force behind the evolution of the sometimes extreme and elaborate genitalia of many species. Sexual selection may arise before and/or after mating, or vary according to other factors such as the social environment. However, bouts of selection are typically considered in isolation. We measured the strength and pattern of selection acting on the length of the male intromittent organ (or processus) in two closely related species of lygaeid seed bug: Lygaeus equestris and Lygaeus simulans. In both species, we measured both pre- and post-copulatory selection. For L. equestris, we also varied the experimental choice design used in mating trials. We found contrasting pre- and post-copulatory selection on processus length in L. equestris. Furthermore, significant pre-copulatory selection was only seen in mating trials in which two males were present. This selection likely arises indirectly due to selection on a correlated trait, as the processus does not interact with the female prior to copulation. In contrast, we were unable to detect significant pre- or post-copulatory selection on processus length in L. simulans. However, a formal meta-analysis of previous estimates of post-copulatory selection on processus length in L. simulans suggests that there is significant stabilising selection across studies, but the strength of selection varies between experiments. Our results emphasise that the strength and direction of sexual selection on genital traits may be multifaceted and can vary across studies, social contexts and different stages of reproduction. SIGNIFICANCE STATEMENT: Animal genitalia vary greatly in size and complexity across species, and selection acting on genital size and shape can be complex. In this study, we show that the length of the penis in two species of seed bug is subject to complex patterns of selection, varying depending on the social context and whether selection is measured before or after mating. In one of the species, we show unexpectedly that penis length is correlated with male mating success, despite the fact that the penis does not interact with the female prior to mating. Our results highlight the fact that genitalia may be subject to both direct and indirect selection at different stages of mating and that to fully understand the evolution of such traits we should combine estimates of selection arising from these multiple episodes.

DNA methylation changes induced by long and short photoperiods in Nasonia.

Many organisms monitor the annual change in day length and use this information for the timing of their seasonal response. However, the molecular mechanisms underlying photoperiodic timing are largely unknown. The wasp Nasonia vitripennis is an emerging model organism that exhibits a strong photoperiodic response: Short autumnal days experienced by females lead to the induction of developmental arrest (diapause) in their progeny, allowing winter survival of the larvae. How female Nasonia control the developmental trajectory of their offspring is unclear. Here, we took advantage of the recent discovery that DNA methylation is pervasive in Nasonia and tested its role in photoperiodism. We used reduced representation bisulfite sequencing (RRBS) to profile DNA methylation in adult female wasps subjected to different photoperiods and identified substantial differential methylation at the single base level. We also show that knocking down DNA methyltransferase 1a (Dnmt1a), Dnmt3, or blocking DNA methylation pharmacologically, largely disrupts the photoperiodic diapause response of the wasps. To our knowledge, this is the first example for a role of DNA methylation in insect photoperiodic timing.

DNA Methylation and Sex Allocation in the Parasitoid Wasp Nasonia vitripennis.

The role of epigenetics in the control and evolution of behavior is being increasingly recognized. Here we test whether DNA methylation influences patterns of adaptive sex allocation in the parasitoid wasp Nasonia vitripennis. Female N. vitripennis allocate offspring sex broadly in line with local mate competition (LMC) theory. However, recent theory has highlighted how genomic conflict may influence sex allocation under LMC, conflict that requires parent-of-origin information to be retained by alleles through some form of epigenetic signal. We manipulated whole-genome DNA methylation in N. vitripennis females using the hypomethylating agent 5-aza-2'-deoxycytidine. Across two replicated experiments, we show that disruption of DNA methylation does not ablate the facultative sex allocation response of females, as sex ratios still vary with cofoundress number as in the classical theory. However, sex ratios are generally shifted upward when DNA methylation is disrupted. Our data are consistent with predictions from genomic conflict over sex allocation theory and suggest that sex ratios may be closer to the optimum for maternally inherited alleles.

Oviposition but Not Sex Allocation Is Associated with Transcriptomic Changes in Females of the Parasitoid Wasp Nasonia vitripennis.

Linking the evolution of the phenotype to the underlying genotype is a key aim of evolutionary genetics and is crucial to our understanding of how natural selection shapes a trait. Here, we consider the genetic basis of sex allocation behavior in the parasitoid wasp Nasonia vitripennis using a transcriptomics approach. Females allocate offspring sex in line with the local mate competition (LMC) theory. Female-biased sex ratios are produced when one or a few females lay eggs on a patch. As the number of females contributing offspring to a patch increases, less female-biased sex ratios are favored. We contrasted the transcriptomic responses of females as they oviposit under conditions known to influence sex allocation: foundress number (a social cue) and the state of the host (parasitized or not). We found that when females encounter other females on a patch or assess host quality with their ovipositors, the resulting changes in sex allocation is not associated with significant changes in whole-body gene expression. We also found that the gene expression changes produced by females as they facultatively allocate sex in response to a host cue and a social cue are very closely correlated. We expanded the list of candidate genes associated with oviposition behavior in Nasonia, some of which may be involved in fundamental processes underlying the ability to facultatively allocate sex, including sperm storage and utilization.