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These authors contributed equally: Gerald S. Wilkinson, Steve Horvath. Correction to: I Nature Communications i https://doi.org/10.1038/s41467-021-21900-2, published online 12 March 2021 The previous version of the Supplementary Information associated with this Article omitted Supplementary Figures 1-6. [Extracted from the article]

These authors contributed equally: Gerald S. Wilkinson, Steve Horvath. The original version of this Article contained an error in the email address of the corresponding author Steve Horvath, which was missing the terminal edu and should be shorvath@mednet.ucla.edu These have been corrected in both the PDF and HTML versions of the Article. [Extracted from the article]

The steps by which isolated populations acquire reproductive incompatibilities remain poorly understood. One potentially important process is postcopulatory sexual selection because it can generate divergence between populations in traits that influence fertilization success after copulation. Here we present a comprehensive analysis of this form of reproductive isolation by conducting reciprocal crosses between variably diverged populations of stalk-eyed flies ( Teleopsis dalmanni). First, we measure seven types of reproductive incompatibility between copulation and fertilization. We then compare fertilization success to hatching success to quantify hybrid inviability. Finally, we determine if sperm competition acts to reinforce or counteract any incompatibilities. We find evidence for multiple incompatibilities in most crosses, including failure to store sperm after mating, failure of sperm to reach the site of fertilization, failure of sperm to fertilize eggs, and failure of embryos to develop. Local sperm have precedence over foreign sperm, but this effect is due mainly to differences in sperm transfer and reduced hatching success. Crosses between recently diverged populations are asymmetrical with regard to the degree and type of incompatibility. Because sexual conflict in these flies is low, postcopulatory sexual selection, rather than antagonistic coevolution, likely causes incompatibilities due to mismatches between male and female reproductive traits. [ABSTRACT FROM AUTHOR]

Coevolution between male and female traits can result from correlated responses to selection or correlated selection on genetically independent traits. This study examines the possibility that traits involved in precopulatory sexual selection may influence the evolution of traits involved in postcopulatory sexual selection due to the existence of correlated selection or correlated responses to selection. Artificial selection on male eye span in Cyrtodiopsis dalmanni, a sexually dimorphic stalk-eyed fly, is used to test for correlated changes in reproductive traits of male and female flies. Flies from replicate lines that had been under selection for 57 generations were matched for age and genotyped at four X-linked microsatellite loci. Egg number and testis size increased with age, but did not differ among lines. Spermathecal areas and duct lengths differed among replicates, but not among selection treatments. Female relative eye span, size of the ventral receptacle and egg size exhibited significant correlated responses to selection on male relative eye span. The absence of any change in sperm length or testis size between lines indicates that changes in female traits are unlikely due to correlated selection mediated by sperm competition. Significant effects of X-linked microsatellite genotypes indicate instead that the correlated responses to selection were due, in part, to X-linked genes in linkage disequilibrium or that exhibit pleiotropy. The presence of nonadditive allelic effects on genetically correlated female traits combined with additive allelic effects on a male ornament provides a previously unrecognized mechanism by which genetic variation could be maintained despite strong sexual selection. [ABSTRACT FROM AUTHOR]

We test the relative rates of evolution of pre- and postzygotic reproductive isolation using eight populations of the sexually dimorphic stalk-eyed flies Cyrtodiopsis dalmanni and C. whitei. Flies from these populations exhibit few morphological differences yet experience strong sexual selection on male eyestalks. To measure reproductive isolation we housed one male and three female flies from within and between these populations in replicate cages and then recorded mating behavior, sperm transfer, progeny production, and hybrid fertility. Using a phylogeny based on partial sequences of two mitochondrial genes, we found that premating isolation, postmating isolation prior to hybrid eclosion, and female hybrid sterility evolve gradually with respect to mitochondrial DNA sequence divergence. In contrast, male hybrid sterility evolves much more rapidly--at least twice as fast as any other form of reproductive isolation. Hybrid sterility, therefore, obeys Haldane's rule. Although some brood sex ratios were female biased, average brood sex ratio did not covary with genetic distance, as would be expected if hybrid inviability obeyed Haldane's rule. The likelihood that forces including sexual selection and intra- and intergenomic conflict may have contributed to these patterns is discussed. [ABSTRACT FROM AUTHOR]

Sperm competition is common in many insect species; however, the mechanisms underlying differences in sperm precedence are not well understood. In the stalk-eyed fly, Cyrtodiopsis whitei (Diptera, Diopsidae), sperm precedence is influenced by the presence of sex chromosome meiotic drive. When drive-carrying males compete with non-driving males for fertilizations within a female, the number of progeny sired by drive males is significantly fewer than predicted by sperm mixing alone. Thus, drive males apparently suffer not only a reduction in the number of viable sperm produced, but also a reduction in sperm competitive ability. In this study, we manipulated the amount and source of seminal fluid and sperm received by females by interrupting copulations before sperm, but after seminal fluid, was transferred. We find that seminal fluid from another male influences the number of progeny sired by a drive-carrying male when both males mate with the same female. Sperm viability staining reveals that sperm from drive males are incapacitated by seminal fluid from other males within the female reproductive tract. These results suggest that multiple mating by females enables seminal fluid products to interact differentially with sperm and may reduce the transmission advantage of the drive chromosome. [ABSTRACT FROM AUTHOR]

Gerald Wilkinson introduces the blood-drinking vampire bats. [ABSTRACT FROM AUTHOR]

Hearing mediates many behaviours critical for survival in echolocating bats, including foraging and navigation. Although most mammals are susceptible to progressive age-related hearing loss, the evolution of biosonar, which requires the ability to hear low-intensity echoes from outgoing sonar signals, may have selected against the development of hearing deficits in bats. Many echolocating bats exhibit exceptional longevity and rely on acoustic behaviours for survival to old age; however, relatively little is known about the ageing bat auditory system. In this study, we used DNA methylation to estimate the ages of wild-caught big brown bats (Eptesicus fuscus) and measured hearing sensitivity in young and ageing bats using auditory brainstem responses (ABRs) and distortion product otoacoustic emissions (DPOAEs). We found no evidence for hearing deficits in bats up to 12.5 years of age, demonstrated by comparable thresholds and similar ABR and DPOAE amplitudes across age groups. We additionally found no significant histological evidence for cochlear ageing, with similar hair cell counts, afferent and efferent innervation patterns in young and ageing bats. Here, we demonstrate that big brown bats show minimal evidence for age-related hearing loss and therefore represent informative models for investigating mechanisms that may preserve hearing function over a long lifetime. [ABSTRACT FROM AUTHOR]

Bats (order Chiroptera) are emerging as instructive animal models for aging studies. Unlike some common laboratory species, they meet a central criterion for aging studies: they live for a long time in the wild or in captivity, for 20, 30, and even >40 years. Healthy aging (i.e., healthspan) in bats has drawn attention to their potential to improve the lives of aging humans due to bat imperviousness to viral infections, apparent low rate of tumorigenesis, and unique ability to repair DNA. At the same time, bat longevity also permits the accumulation of age‐associated systemic pathologies that can be examined in detail and manipulated, especially in captive animals. Research has uncovered additional and critical advantages of bats. In multiple ways, bats are better analogs to humans than are rodents. In this review, we highlight eight diverse areas of bat research with relevance to aging: genome sequencing, telomeres, and DNA repair; immunity and inflammation; hearing; menstruation and menopause; skeletal system and fragility; neurobiology and neurodegeneration; stem cells; and senescence and mortality. These examples demonstrate the broad relevance of the bat as an animal model and point to directions that are particularly important for human aging studies. [ABSTRACT FROM AUTHOR]

Abstract: Among mammals, bats exhibit extreme variation in sociality, with some species living largely solitary lives while others form colonies of more than a million individuals. Some tropical species form groups during the day that persist throughout the year while many temperate species only gather into groups during hibernation or parturition. How groups form and then persist has now been described for a number of species, but the degree to which kinship explains patterns of association has never been quantified across species. Here, we use social network analysis and genetic data to determine the extent to which relatedness contributes to associations among individuals estimated from free-ranging animals across nine species from four families of bats. Network analysis reveals that all species show evidence of emergent social structure. Variation in the strength of the relationship between genetic relatedness and social association appears to be related to the degree of roost switching, i.e., species in which individuals change roosts frequently tend to exhibit higher levels of association among relatives. Sex-biased dispersal determines whether associations were between male or female relatives. The strength of associations among kin does not predict known occurrence of complex behaviors, such as dominance or various types of cooperation, indicating that kinship is not a prerequisite for social complexity in bats.Significance statement: The number of differentiated relationships has been proposed as a way to measure social complexity. Among primates, relationships can be differentiated on the basis of rank, age, kinship, or association. Application of this approach to other groups of mammals that vary in sociality could help reveal ecological, behavioral, or cognitive similarities and differences between species. As a first step toward this approach, we used social network analysis on long-term individual records and estimated relatedness using genetic markers for nine species of bats. We confirmed nonrandom emergent social structure in all species. Kinship was predictive of social association among individuals of the same sex in a few species, but largely independent of the occurrence of complex behaviors, such as dominance among males or cooperation among females. Complex social behavior in bats appears to require frequent interactions among a small number of individuals that roost together for multiple years. [ABSTRACT FROM AUTHOR]

Chemical signals are ubiquitous, but often overlooked as potentially important for conveying information relevant for sexual selection. The male greater spear-nosed bat, Phyllostomus hastatus, possesses a sexually dimorphic gland on the chest that produces an odoriferous secretion. Here, we investigate the potential for this glandular secretion to act as a sexually selected olfactory signal by examining gland activity in and out of the mating season and determining if variation in its chemical composition reflects variation in male mating status or attributes of the individual. Based on gas chromatography-mass spectrometry (GC-MS) measurements of samples collected from wild bats roosting in caves in Trinidad, West Indies, we find that males that defend and roost with groups of females (harem holders) have significantly different chemical profiles from males found roosting in all male groups (bachelors). Additionally, profiles differed significantly among individuals. Taken together, these results suggest that this chemical signal has the potential to communicate both mating status and individual identity and thus could be used to mediate interactions among individuals within this harem-based social mating system. [ABSTRACT FROM AUTHOR]

Stalk-eyed flies in the genus Teleopsis carry selfish genetic elements that induce sex ratio (SR) meiotic drive and impact the fitness of male and female carriers. Here, we assemble and describe a chromosome-level genome assembly of the stalk-eyed fly, Teleopsis dalmanni , to elucidate patterns of divergence associated with SR. The genome contains tens of thousands of transposable element (TE) insertions and hundreds of transcriptionally and insertionally active TE families. By resequencing pools of SR and ST males using short and long reads, we find widespread differentiation and divergence between XSR and XST associated with multiple nested inversions involving most of the SR haplotype. Examination of genomic coverage and gene expression data revealed seven X-linked genes with elevated expression and coverage in SR males. The most extreme and likely drive candidate involves an XSR-specific expansion of an array of partial copies of JASPer, a gene necessary for maintenance of euchromatin and associated with regulation of TE expression. In addition, we find evidence for rapid protein evolution between XSR and XST for testis expressed and novel genes, that is, either recent duplicates or lacking a Dipteran ortholog, including an X-linked duplicate of maelstrom , which is also involved in TE silencing. Overall, the evidence suggests that this ancient XSR polymorphism has had a variety of impacts on repetitive DNA and its regulation in this species. [ABSTRACT FROM AUTHOR]

Comparative studies of language are difficult because few language precursors are recognized. In this paper we propose a framework for designing experiments that test for structural and semantic patterns indicative of simple or complex grammars as originally described by Chomsky. We argue that a key issue is whether animals can recognize full recursion, which is the hallmark of context-free grammar. We discuss limitations of recent experiments that have attempted to address this issue, and point out that experiments aimed at detecting patterns that follow a Fibonacci series have advantages over other artificial context-free grammars. We also argue that experiments using complex sequences of behaviors could, in principle, provide evidence for fully recursive thought. Some of these ideas could also be approached using artificial life simulations, which have the potential to reveal the types of evolutionary transitions that could occur over time. Because the framework we propose has specific memory and computational requirements, future experiments could target candidate genes with the goal of revealing the genetic underpinnings of complex cognition. [ABSTRACT FROM AUTHOR]

Language has been considered by many to be uniquely human. Numerous theories for how it evolved have been proposed but rarely tested. The articles in this theme issue consider the extent to which aspects of language, such as vocal learning, phonology, syntax, semantics, intentionality, cognition and neurobiological adaptations, are shared with other animals. By adopting a comparative approach, insights into the mechanisms and origins of human language can be gained. While points of agreement exist among the authors, conflicting viewpoints are expressed on several issues, such as the presence of proto-syntax in animal communication, the neural basis of the Merge operation, and the neurogenetic changes necessary for vocal learning. Future comparative research in animal communication has the potential to teach us even more about the evolution, neurobiology and cognitive basis of human language. This article is part of the theme issue 'What can animal communication teach us about human language?' [ABSTRACT FROM AUTHOR]

Artificial selection offers a powerful tool for the exploration of how selection and development shape the evolution of morphological scaling relationships. An emerging approach models the expression and evolution of morphological scaling relationships as a function of variation among individuals in the developmental mechanisms that regulate trait growth. These models posit the existence of genotype-specific morphological scaling relationships that are unseen or "cryptic." Within-population allelic variation at growth-regulating loci determines how these individual cryptic scaling relationships are distributed, and exposure to environmental factors that affect growth determines the size phenotype expressed by each individual on their cryptic, genotype-specific scaling relationship. These models reveal that evolution of the intercept and slope of the population -level static allometry is determined, often in counterintuitive ways, largely by the shape of the distribution of these underlying individual -level scaling relationships. Here we review this modeling framework and present the wing-body size individual cryptic scaling relationships from a population of Drosophila melanogaster. To determine how these models might inform interpretation of published work on scaling relationship evolution, we review studies where artificial selection was applied to alter the parameters of population-level static allometries. Finally, motivated by our review, we outline areas in need of empirical work and describe a research program to address these topics; the approach includes describing the distribution of individual cryptic scaling relationships across populations and environments, empirical testing of the model's predictions, and determining the effects of environmental heterogeneity on realized trait distributions and how this affects allometry evolution. [ABSTRACT FROM AUTHOR]