The neuropeptide drosulfakinin enhances choosiness and protects males from the aging effects of social perception.

The motivation to reproduce is a potent natural drive, and the social behaviors that induce it can severely impact animal health and lifespan. Indeed, in Drosophila males, accelerated aging associated with reproduction arises not from the physical act of courtship or copulation but instead from the motivational drive to court and mate. To better understand the mechanisms underlying social effects on aging, we studied male choosiness for mates. We found that increased activity of insulin-producing cells (IPCs) of the fly brain potentiated choosiness without consistently affecting courtship activity. Surprisingly, this effect was not caused by insulins themselves, but instead by drosulfakinin (DSK), another neuropeptide produced in a subset of the IPCs, acting through one of the two DSK receptors, CCKLR-17D1. Activation of Dsk+ IPC neurons also decreased food consumption, while activation of Dsk+ neurons outside of IPCs affected neither choosiness nor feeding, suggesting an overlap between Dsk+neurons modulating choosiness and those influencing satiety. Broader activation of Dsk+ neurons (both within and outside of the IPCs) was required to rescue the detrimental effect of female pheromone exposure on male lifespan, as was the function of both DSK receptors. The same broad set of Dsk+ neurons was found to reinforce normally aversive feeding interactions, but only after exposure to female pheromones, suggesting that perception of the opposite sex gates rewarding properties of these neurons. We speculate that broad Dsk+ neuron activation is associated with states of satiety and social experience, which under stressful conditions is rewarding and beneficial for lifespan.

Measuring the Efficiency of Purging by non-random Mating in Human Populations.

Human populations harbor a high concentration of deleterious genetic variants. Here, we tested the hypothesis that non-random mating practices affect the distribution of these variants, through exposure in the homozygous state, leading to their purging from the population gene pool. To do so, we produced whole-genome sequencing data for two pairs of Asian populations exhibiting different alliance rules and rates of inbreeding, but with similar effective population sizes. The results show that populations with higher rates of inbred matings do not purge deleterious variants more efficiently. Purging therefore has a low efficiency in human populations, and different mating practices lead to a similar mutational load.

No neonates without adults: A review of adult black soldier fly biology, Hermetia illucens (Diptera: Stratiomyidae): A review of adult black soldier fly biology, Hermetia illucens (Diptera: Stratiomyidae).

With the potential to process the world's agricultural and food waste, provide sustainable fodder for livestock, aquaculture, and pet animals, as well as act as a source of novel biomolecules, the black soldier fly, Hermetia illucens, has been launched into the leading position within the insects as feed industry. Fulfilment of these goals, however, requires mass-rearing facilities to have a steady supply of neonate larvae, which in-turn requires an efficient mating process to yield fertile eggs; yet, little is known about adult reproductive behavior, nor what physiological factors lead to its emergence. Moreover, fertile egg production tends to be highly variable in colony. Therefore, this review brings together what is currently known of the organismal biology of H. illucens, compiling information on adult morphology, physiology, biogeography, genomics, and behavioral ecology. As a holistic synthesis, it highlights several directions of interest for research to follow.

Assortative mating on blood type: Evidence from one million Chinese pregnancies.

Blood type is one of the most fundamental phenotypes in biological, medical, and psychological studies. Using a unique dataset of one million Chinese pregnancies, we find strong evidence from a group of statistical tests for assortative mating on blood type. After controlling for anthropometric and socioeconomic confounders, assortative mating remains robust.

The evolution of mating preferences for genetic attractiveness and quality in the presence of sensory bias.

The aesthetic preferences of potential mates have driven the evolution of a baffling diversity of elaborate ornaments. Which fitness benefit-if any-choosers gain from expressing such preferences is controversial, however. Here, we simulate the evolution of preferences for multiple ornament types (e.g., "Fisherian," "handicap," and "indicator" ornaments) that differ in their associations with genes for attractiveness and other components of fitness. We model the costs of preference expression in a biologically plausible way, which decouples costly mate search from cost-free preferences. Ornaments of all types evolved in our model, but their occurrence was far from random. Females typically preferred ornaments that carried information about a male's quality, defined here as his ability to acquire and metabolize resources. Highly salient ornaments, which key into preexisting perceptual biases, were also more likely to evolve. When males expressed quality-dependent ornaments, females invested readily in costly mate search to locate preferred males. In contrast, the genetic benefits associated with purely arbitrary ornaments were insufficient to sustain highly costly mate search. Arbitrary ornaments could nonetheless "piggyback" on mate-search effort favored by other, quality-dependent ornaments. We further show that the potential to produce attractive male offspring ("sexy sons") can be as important as producing offspring of high general quality ("good genes") in shaping female preferences, even when preferred ornaments are quality dependent. Our model highlights the importance of mate-search effort as a driver of aesthetic coevolution.

Assortative mating enhances postzygotic barriers to gene flow via ancestry bundling.

Hybridization and subsequent genetic introgression are now known to be common features of the histories of many species, including our own. Following hybridization, selection often purges introgressed DNA genome-wide. While assortative mating can limit hybridization in the first place, it is also known to play an important role in postzygotic selection against hybrids and, thus, the purging of introgressed DNA. However, this role is usually thought of as a direct one: a tendency for mates to be conspecific reduces the sexual fitness of hybrids, reducing the transmission of introgressed ancestry. Here, we explore a second, indirect role of assortative mating as a postzygotic barrier to gene flow. Under assortative mating, parents covary in their ancestry, causing ancestry to be "bundled" in their offspring and later generations. This bundling effect increases ancestry variance in the population, enhancing the efficiency with which postzygotic selection purges introgressed DNA. Using whole-genome simulations, we show that the bundling effect can comprise a substantial portion of mate choice's overall effect as a postzygotic barrier to gene flow. We then derive a simple method for estimating the impact of the bundling effect from standard metrics of assortative mating. Applying this method to data from a diverse set of hybrid zones, we find that the bundling effect increases the purging of introgressed DNA by between 1.2-fold (in a baboon system with weak assortative mating) and 14-fold (in a swordtail system with strong assortative mating). Thus, assortative mating's bundling effect contributes substantially to the genetic isolation of species.

Meta-analytical evidence that males prefer virgin females.

Males are often predicted to prefer virgin over non-virgin females because of the reduced risk of sperm competition. Does this prediction hold across studies? Our systematic meta-analysis of 138 studies, mainly conducted in invertebrates, confirms that males generally prefer virgin females. However, males preferred virgin females even in species with last male sperm precedence, suggesting that sperm competition alone does not drive male preferences. Furthermore, our results suggest that males may reject mated females even when no alternative exists. Preference for virgins is unlikely to influence female reproductive success since virginity cannot be selected for, but strong preference for virgin females could swamp or reinforce selection on other traits. Our results add to growing evidence that males are not indiscriminate in mating. However, given the unexplained heterogeneity in effect sizes, we urge caution in assuming that males will prefer virgins and recommend considering the natural context of mating decisions.

The Evolution of Mate Attachment.

AbstractWhether natural selection leads to attachment in monogamous pair bonds has seldom been addressed. Operationally defining attachment as a behavioral modifier that decreases divorce probability with pair duration, we develop a model for the evolution of attachment. If divorce (the ending of a pair bond when both individuals survive to the next breeding season) is more likely to occur out of poor-quality reproductive opportunities (i.e., poor territory or low-quality mate), individuals in experienced pairs are more likely to be found in high-quality opportunities. Consequently, when divorce decisions occur using imperfect information from reproductive success, pair duration provides individuals with information about the quality of their reproductive opportunity and attachment can evolve. We show that high survival rates, divorce propensities, and probabilities of nest failure favor the evolution of attachment. Attachment is also more likely to evolve when individuals can directly assess the quality of their reproductive opportunity (as opposed to relying on imperfect information from reproductive success), when the quality of the reproductive opportunity has adult survival ramifications, and when divorce coevolves with attachment. We show that our core conclusions are robust to a variety of assumptions using individual-based simulations. Our results clarify how attachment can be adaptive and suggest that studying pair bonds as dynamic entities is a promising avenue for future work.

Mate choice in the brain: species differ in how male traits 'turn on' gene expression in female brains.

Mate choice plays a fundamental role in speciation, yet we know little about the molecular mechanisms that underpin this crucial decision-making process. Stickleback fish differentially adapted to limnetic and benthic habitats are reproductively isolated and females of each species use different male traits to evaluate prospective partners and reject heterospecific males. Here, we integrate behavioural data from a mate choice experiment with gene expression profiles from the brains of females actively deciding whether to mate. We find substantial gene expression variation between limnetic and benthic females, regardless of behavioural context, suggesting general divergence in constitutive gene expression patterns, corresponding to their genetic differentiation. Intriguingly, female gene co-expression modules covary with male display traits but in opposing directions for sympatric populations of the two species, suggesting male displays elicit a dynamic neurogenomic response that reflects known differences in female preferences. Furthermore, we confirm the role of numerous candidate genes previously implicated in female mate choice in other species, suggesting evolutionary tinkering with these conserved molecular processes to generate divergent mate preferences. Taken together, our study adds important new insights to our understanding of the molecular processes underlying female decision-making critical for generating sexual isolation and speciation.

Sexual conflict and sexual networks in bed bugs: the fitness cost of traumatic insemination, female avoidance and male mate choice.

Sexual conflict is prevalent among animals and is primarily caused by the fact that the optimal mating rates are often higher in males than in females. While there is a growing appreciation that females can also gain from multiple matings, we still know relatively little about which sex controls the observed mating rates and how close it is to the optimal female mating rates. To address this issue, we tracked female bed bugs (Cimex lectularius) inseminated daily versus weekly and found that weekly inseminated females lived longer and produced over 50% more offspring. In a follow-up experiment employing a social network framework, we placed 24 bed bugs into a semi-naturalistic arena and recorded all sexual interactions. While recently inseminated females did not avoid males more often, they were more frequently rejected by males. Finally, we tracked avoidance behaviour in a single cohort of female bed bugs as they received six successive daily inseminations. Avoidance rates increased and insemination durations decreased with increasing number of prior inseminations. Overall, our results indicate high costs of polyandry. Although females possess some plastic avoidance strategies, the observed rates of insemination fall closer to the male rather than female optimum.

A reformulation of Fisher's runaway identifies the heritability of mate choices as a key parameter and highlights limitations of the hypothesis.

Fisher proposed that female preference for mates with extreme traits could evolve as an essentially arbitrary outcome of a self-reinforcing process. Although Fisher's runaway has been shown to be a theoretical possibility, it is not clear whether it occurs in real populations, in part because existing models express the necessary conditions in terms of parameters that would be nearly impossible to estimate in the wild. Here, I reformulate models of the runaway in terms of two estimable parameters, the heritability and phenotypic variance of realized mate choices. Higher values of both quantities make the runaway more likely. In the most realistic model considered, in which mate choices are based on a mixture of absolute and relative criteria, a runaway cannot occur unless mate choice increases the variance of the male trait, which seems incompatible with the strong directional mating preferences typically observed in polygynous species. Even in the most favourable case for the runaway, purely relative preference without direct selection on preference, a substantial heritability of realized mate choices would be required if there is moderately strong stabilizing selection on the male trait. These results cast some doubt on whether the runaway is a plausible outcome in natural populations.

Mate-choice copying accelerates species range expansion.

Mate-choice copying is a type of social learning in which females can change their mate preference after observing the choice of others. This behaviour can potentially affect population evolution and ecology, namely through increased dispersal and reduced local adaptation. Here, we simulated the effects of mate-choice copying in populations expanding across an environmental gradient to understand whether it can accelerate or retard the expansion process. Two mate-choice copying strategies were used: (i) when females target a single individual and (ii) when females target similar individuals. We also simulated cases where the male trait singled out by females with mate choice maps perfectly onto his genotype or is influenced by genotype-by-environment interactions. These rules have different effects on the results. When a trait is determined by genotype alone, populations where copier females target all similar males expand faster and the number of potential copiers increased. However, when preference is determined by genotype-by-environment interactions, populations where copier females target a single male had higher dispersal and also expand faster, but the potential number of copiers decreases. The results show that mate-choice copying can accelerate the expansion process, although its adaptiveness depends on the information animals use in different contexts.

Spider dung beetles: coordinated cooperative transport without a predefined destination.

Cooperative transport allows for the transportation of items too large for the capacity of a single individual. Beyond humans, it is regularly employed by ants and social spiders where two or more individuals, with more or less coordinated movements, transport food to a known destination. In contrast to this, pairs of male and female dung beetles successfully transport brood balls to a location unknown to either party at the start of their common journey. We found that, when forced to overcome a series of obstacles in their path, transport efficiency of pairs of beetles was higher than of solo males. To climb tall obstacles with their common ball of dung, the female assisted the leading male in lifting the ball by steadying and pushing it upwards in a 'headstand' position during the climb initiation. Finally, we show that pairs were faster than single beetles in climbing obstacles of different heights. Our results suggest that pairs of Sisyphus beetles cooperate in the transportation of brood balls with coordinated movements, where the male steers and the female primarily assists in lifting the ball. Taken together, this is to our knowledge, the first quantitative study of cooperative food transport without a known goal to aim for.

Sexually selected differences in warbler plumage are related to a putative inversion on the Z chromosome.

Large structural variants in the genome, such as inversions, may play an important role in producing population structure and local adaptation to the environment through suppression of recombination. However, relatively few studies have linked inversions to phenotypic traits that are sexually selected and may play a role in reproductive isolation. Here, we found that geographic differences in the sexually selected plumage of a warbler, the common yellowthroat (Geothlypis trichas), are largely due to differences in the Z (sex) chromosome (males are ZZ), which contains at least one putative inversion spanning 40% (31/77 Mb) of its length. The inversions on the Z chromosome vary dramatically east and west of the Appalachian Mountains, which provides evidence of cryptic population structure within the range of the most widespread eastern subspecies (G. t. trichas). In an eastern (New York) and western (Wisconsin) population of this subspecies, female prefer different male ornaments; larger black facial masks are preferred in Wisconsin and larger yellow breasts are preferred in New York. The putative inversion also contains genes related to vision, which could influence mating preferences. Thus, structural variants on the Z chromosome are associated with geographic differences in male ornaments and female choice, which may provide a mechanism for maintaining different patterns of sexual selection in spite of gene flow between populations of the same subspecies.

The effects of intersexual interactions on survival can drive the evolution of female ornaments in the absence of mate limitation.

The evolution of sexual ornaments in animals is typically attributed to reproductive competition. However, sexual ornaments also arise in contexts where the ornamented sex is neither mate nor gamete limited, and explanations for ornamentation in these cases remain incomplete. In many species, particularly those with slow life histories, lifetime reproductive success depends more strongly on adult survival than fecundity, and survival can depend on intersexual interactions. We develop a population genetic model to investigate how the effect of intersexual interactions on survival may contribute to ornament evolution in the absence of competition for mates. Using female ornamentation in polygynous mating systems as a case study, we show that, indeed, ornaments can evolve when the ornament functions to modify interactions with males in ways that enhance a female's own survival. The evolutionary dynamics depend qualitatively on the specific behavioral mechanism by which the ornament modifies social interactions. In all cases, the ornament's long-term persistence is ultimately determined by the coevolution of the male locus that determines how males affect female survival. We outline the scenarios that are most likely to favor the evolution of female ornaments through the effects of intersexual interactions on survival, and we urge empirical researchers to consider the potential for this social selection mechanism to shape traits of interest across taxa.

Sympatry and parapatry among rocky reef cichlids of Lake Victoria explained by female mating preferences.

Work on the Lake Victoria cichlids Pundamilia nyererei (red dorsum males, deeper water), Pundamilia pundamilia (blue males, shallower water) and related species pairs has provided insights into processes of speciation. Here, we investigate the female mating behaviour of 5 Pundamilia species and 4 of their F1 hybrids through mate choice trials and paternity testing. Complete assortative mating was observed among all sympatric species. Parapatric species with similar depth habitat distributions interbred whereas other parapatric and allopatric species showed complete assortative mating. F1 hybrids mated exclusively with species accepted by females of the parental species. The existence of complete assortative mating among some currently allopatric species suggests that pre-existing mating barriers could be sufficient to explain current patterns of co-existence, although, of course, many other factors may be involved. Regardless of the mechanism, mating preferences may influence species distribution in potentially hybridizing taxa, such as in the adaptive radiation of cichlid fish. We suggest that this at least partly explains why some species fail to establish breeding populations in locations where they are occasionally recorded. Our results support the notion that the mating preferences of potentially cross-breeding species ought to be included in coexistence theory.

The quantitative genetic basis of variation in sexual versus non-sexual butterfly wing colouration: autosomal, Z-linked, and maternal effects.

Viability indicator traits are expected to be integrated extensively across the genome yet sex-limited to ensure that any benefits are sexually concordant. Understanding how such expectations are accommodated requires elucidating the quantitative genetic architecture of candidate traits in and across the sexes. Here we applied an animal modelling approach to partition the autosomal, allosomal, and direct maternal bases of variation in sexual versus non-sexual dorsal wing colouration in the butterfly Eurema hecabe. The sexual colour trait-coherently scattered ultraviolet that is under strong directional selection due to female choice-is brighter and more expansive in males, and overlays non-sexual pigmentary yellow markings that otherwise dominate both wing surfaces in each sex. Our modelling estimated high and sexually equivalent autosomal variances for ultraviolet reflectance (furnishing h2 ~ 0.58 overall and ~0.75 in males), accompanied by smaller but generally significant Z-linked and maternal components. By contrast, variation in non-sexual yellow was largely attributed to Z-linked sources. Intersexual genetic correlations based upon the major source of variation in each trait were high and not different from 1.0, implying regulation by a pool of genes common to each sex. An expansive autosomal basis for ultraviolet is consistent with its hypothesized role as a genome-wide viability indicator and ensures that both sons and daughters will inherit their father's attractiveness.

Beyond simple vs. complex: exploring the nuanced and unexpected effects of spatial environmental complexity on mating patterns and female fecundity.

The features of the physical environment set the stage upon which sexual selection operates, and consequently can have a significant impact on variation in realized individual fitness, and influence a population's evolutionary trajectory. This phenomenon has been explored empirically in several studies using fruit flies (Drosophila melanogaster) which have found that changing the spatial complexity of the mating environment influenced male-female interaction dynamics, (re)mating rates, and realized female fecundities. However, these studies did not explore mating patterns, which can dramatically alter the genetic composition of the next generation, and frequently only compared a single, small "simple" environment to a single larger "complex" environment. While these studies have shown that broadly changing the characteristics of the environment can have big effects on reproductive dynamics, the plasticity of this outcome to more subtle changes has not been extensively explored. Our study set out to compare patterns of mating and courtship between large- and small-bodied males and females, and female fecundities in both a simple environment and 2 distinctly different spatially complex environments. We found that realized offspring production patterns differed dramatically between all 3 environments, indicating that the effects of increasing spatial complexity on mating outcomes are sensitive to the specific type of environmental complexity. Furthermore, we observed female fecundities were higher for flies in both complex environments compared those in the simple environment, supporting its role as a mediator of sexual conflict. Together, these results show that the union of gametes within a population can be greatly influenced by the specific spatial features of the environment and that while some outcomes of increased environmental complexity are likely generalizable, other phenomena such as mating patterns and courtship rates may vary from one complex environment to another.

Within-population variation in preference functions reveals substantial among-female disagreement in mate assessment.

The mate choice behaviours of females can greatly affect patterns of reproductive success in males and influence the evolution of sexually selected male traits. Population-level estimates of display preferences may provide an accurate estimate of the strength and direction of selection by female choice if all females in the population show homogeneous preferences. However, population-level estimates may yield misleading estimates if there is within-population variation in mate preferences. While it is increasingly clear that the latter situation is common in nature, empirical data on the magnitude of variation in female preferences are required to improve our current understanding of its potential evolutionary consequences. We explored variations in female preference functions for 3 male call properties in a treefrog. We document substantial within-population variation not only in peak preferences but also in preference function shape (open, closed, flat), with at best 62% of females sharing a preference function shape with the respective population curve. Our findings suggest that population curves may accurately capture the direction of sexual selection, but depending on the properties of the constituting individual functions they may over- or underestimate the strength of selection. Particularly population estimates suggesting weak selection may in fact hide the presence of individual females with strong but opposing preferences. Moreover, due to the high within-population variation in both peak preferences and preference function shapes, the population functions drastically underestimate the predicted variation in male mating success in the population.

Divergent warning patterns influence male and female mating behaviours in a tropical butterfly.

Traits under divergent ecological selection that also function during mating can be important in maintaining species boundaries. Few studies have considered mutual mate choice, where both males and females base mating decisions on the same trait. Wing colouration in Heliconius butterflies evolved as a warning signal but also functions as a mating cue. We investigated the contribution of visual preference to assortative mating in an aposematic butterfly Heliconius cydno in the context of reproductive isolation with its sympatric, visually distinct relative Heliconius melpomene. Heliconius cydno have conspicuous white bands on their forewings, whereas those of H. melpomene are red in colour. We predicted that both sexes of H. cydno contributed to assortative mating by exhibiting visual preference towards conspecific wing colouration. We analysed published and new data from preference experiments, in which males were presented with conspecific and H. melpomene females. We also recorded female responses and mating outcomes in choice experiments, involving conspecific males with either the original white or artificially painted red forewing bands. Both sexes of H. cydno responded more positively towards the conspecific colouration, and males strongly preferred females of its own colours. In contrast, male colouration did not predict mating outcomes in female choice experiments. As courtships are initiated by males in butterflies, our findings suggest that female visual preference might be of secondary importance in H. cydno. Our data also suggest that the contribution of visual preference to reproductive isolation might be unequal between H. cydno and its sympatric relative H. melpomene.