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1. Sex-specific natural selection on SNPs in Silene latifolia

   https://doi.org/10.1002/evl3.283  

   Delph, Lynda F. ; Brown, Keely E. ; Ríos, Luis Diego ; Kelly, John K. ( August 2022 , Evolution Letters)

   Selection that acts in a sex-specific manner causes the evolution of sexual dimorphism. Sex-specific phenotypic selection has been demonstrated in many taxa and can be in the same direction in the two sexes (differing only in magnitude), limited to one sex, or in opposing directions (antagonistic). Attempts to detect the signal of sex-specific selection from genomic data have confronted numerous difficulties. These challenges highlight the utility of “direct approaches,” in which fitness is predicted from individual genotype within each sex. Here, we directly measured selection on Single Nucleotide Polymorphisms (SNPs) in a natural population of the sexually dimorphic, dioecious plant, Silene latifolia. We measured flowering phenotypes, estimated fitness over one reproductive season, as well as survival to the next year, and genotyped all adults and a subset of their offspring for SNPs across the genome. We found that while phenotypic selection was congruent (fitness covaried similarly with flowering traits in both sexes), SNPs showed clear evidence for sex-specific selection. SNP-level selection was particularly strong in males and may involve an important gametic component (e.g., pollen competition). While the most significant SNPs under selection in males differed from those under selection in females, paternity selection showed a highly polygenic tradeoff with female survival. Alleles that increased male mating success tended to reduce female survival, indicating sexual antagonism at the genomic level. Perhaps most importantly, this experiment demonstrates that selection within natural populations can be strong enough to measure sex-specific fitness effects of individual loci.

   Males and females typically differ phenotypically, a phenomenon known as sexual dimorphism. These differences arise when selection on males differs from selection on females, either in magnitude or direction. Estimated relationships between traits and fitness indicate that sex-specific selection is widespread, occurring in both plants and animals, and explains why so many species exhibit sexual dimorphism. Finding the specific loci experiencing sex-specific selection is a challenging prospect but one worth undertaking given the extensive evolutionary consequences. Flowering plants with separate sexes are ideal organisms for such studies, given that the fitness of females can be estimated by counting the number of seeds they produce. Determination of fitness for males has been made easier as thousands of genetic markers can now be used to assign paternity to seeds. We undertook just such a study in S. latifolia, a short-lived, herbaceous plant. We identified loci under sex-specific selection in this species and found more loci affecting fitness in males than females. Importantly, loci with major effects on male fitness were distinct from the loci with major effects on females. We detected sexual antagonism only when considering the aggregate effect of many loci. Hence, even though males and females share the same genome, this does not necessarily impose a constraint on their independent evolution.

    

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2. Zebrafish gonad mutant models reveal neuroendocrine mechanisms of brain sexual dimorphism and male mating behaviors of different brain regions

   https://doi.org/10.1186/s13293-023-00534-7  

   Dai, Xiangyan ; Pradhan, Ajay ; Liu, Jiao ; Liu, Ruolan ; Zhai, Gang ; Zhou, Linyan ; Dai, Jiyan ; Shao, Feng ; Yuan, Zhiyong ; Wang, Zhijian ; et al ( August 2023 , Biology of Sex Differences)

   Sexually dimorphic mating behaviors differ between sexes and involve gonadal hormones and possibly sexually dimorphic gene expression in the brain. However, the associations among the brain, gonad, and sexual behavior in teleosts are still unclear. Here, we utilized germ cells-freetdrd12knockout (KO) zebrafish, and steroid synthesis enzymecyp17a1-deficient zebrafish to investigate the differences and interplays in the brain–gonad–behavior axis, and the molecular control of brain dimorphism and male mating behaviors.

   Tdrd12^+/−;cyp17a1^+/−double heterozygous parents were crossed to obtaintdrd12^−/−;cyp17a1^+/+(tdrd12 KO),tdrd12^+/+;cyp17a1^−/−(cyp17a1 KO), andtdrd12^−/−;cyp17a1^−/−(double KO) homozygous progenies. Comparative analysis of mating behaviors were evaluated using Viewpoint zebrafish tracking software and sexual traits were thoroughly characterized based on anatomical and histological experiments in these KOs and wild types. The steroid hormone levels (testosterone, 11-ketotestosterone and 17β-estradiol) in the brains, gonads, and serum were measured using ELISA kits. To achieve a higher resolution view of the differences in region-specific expression patterns of the brain, the brains of these KOs, and control male and female fish were dissected into three regions: the forebrain, midbrain, and hindbrain for transcriptomic analysis.

   Qualitative analysis of mating behaviors demonstrated thattdrd12^−/−fish behaved in the same manner as wild-type males to trigger oviposition behavior, whilecyp17a1^−/−and double knockout (KO) fish did not exhibit these behaviors. Based on the observation of sex characteristics, mating behaviors and hormone levels in these mutants, we found that the maintenance of secondary sex characteristics and male mating behavior did not depend on the presence of germ cells; rather, they depended mainly on the 11-ketotestosterone and testosterone levels secreted into the brain–gonad regulatory axis. RNA-seq analysis of different brain regions revealed that the brain transcript profile oftdrd12^−/−fish was similar to that of wild-type males, especially in the forebrain and midbrain. However, the brain transcript profiles ofcyp17a1^−/−and double KO fish were distinct from those of wild-type males and were partially biased towards the expression pattern of the female brain. Our results revealed important candidate genes and signaling pathways, such as synaptic signaling/neurotransmission, MAPK signaling, and steroid hormone pathways, that shape brain dimorphism and modulate male mating behavior in zebrafish.

   Our results provide comprehensive analyses and new insights regarding the endogenous interactions in the brain–gonad–behavior axis. Moreover, this study revealed the crucial candidate genes and neural signaling pathways of different brain regions that are involved in modulating brain dimorphism and male mating behavior in zebrafish, which would significantly light up the understanding the neuroendocrine and molecular mechanisms modulating brain dimorphism and male mating behavior in zebrafish and other teleost fish.

    

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3. How female × male and male × male interactions influence competitive fertilization in Drosophila melanogaster

   https://doi.org/10.1002/evl3.193  

   Lüpold, Stefan ; Reil, Jonathan Bradley ; Manier, Mollie K. ; Zeender, Valérian ; Belote, John M. ; Pitnick, Scott ( October 2020 , Evolution Letters)

   How males and females contribute to joint reproductive success has been a long-standing question in sexual selection. Under postcopulatory sexual selection, paternity success is predicted to derive from complex interactions among females engaging in cryptic female choice and males engaging in sperm competition. Such interactions have been identified as potential sources of genetic variation in sexually selected traits but are also expected to inhibit trait diversification. To date, studies of interactions between females and competing males have focused almost exclusively on genotypes and not phenotypic variation in sexually selected traits. Here, we characterize within- and between-sex interactions in Drosophila melanogaster using isogenic lines with heritable variation in both male and female traits known to influence competitive fertilization. We confirmed, and expanded on, previously reported genotypic interactions within and between the sexes, and showed that several reproductive events, including sperm transfer, female sperm ejection, and sperm storage, were explained by two- and three-way interactions among sex-specific phenotypes. We also documented complex interactions between the lengths of competing males’ sperm and the female seminal receptacle, which are known to have experienced rapid female-male co-diversification. Our results highlight the nonindependence of sperm competition and cryptic female choice and demonstrate that complex interactions between the sexes do not limit the ability of multivariate systems to respond to directional sexual selection.

    

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4. A learning experience elicits sex‐dependent neurogenomic responses in Bicyclus anynana butterflies

   https://doi.org/10.1111/mec.16920  

   Ernst, David A. ; Agcaoili, Gabrielle A. ; Merrill, Abbigail N. ; Westerman, Erica L. ( March 2023 , Molecular Ecology)

   Sexually dimorphic behaviour is pervasive across animals, with males and females exhibiting different mate selection, parental care, foraging, dispersal, and territorial strategies. However, the genetic underpinnings of sexually dimorphic behaviours are poorly understood. Here we investigate gene networks and expression patterns associated with sexually dimorphic imprinting‐like learning in the butterflyBicyclus anynana. In this species, both males and females learn visual preferences, but learn preferences for different traits and use different signals as salient, unconditioned cues. To identify genes and gene networks associated with this behaviour, we examined gene expression profiles of the brains and eyes of male and female butterflies immediately post training and compared them to the same tissues of naïve individuals. We found more differentially expressed genes and a greater number of associated gene networks in the eyes, indicating a role of the peripheral nervous system in visual imprinting‐like learning. Females had higher chemoreceptor expression levels than males, supporting the hypothesized sexual dimorphic use of chemical cues during the learning process. In addition, genes that influenceB. anynanawing patterns (sexual ornaments), such asinvected,spalt, andapterous, were also differentially expressed in the brain and eye, suggesting that these genes may influence both sexual ornaments and the preferences for these ornaments. Our results indicate dynamic and sex‐specific responses to social scenario in both the peripheral and central nervous systems and highlight the potential role of wing patterning genes in mate preference and learning across the Lepidoptera.

    

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5. Vascularization underlies differences in sexually selected skin coloration in a wild primate

   https://doi.org/10.1111/mec.17026  

   DeLacey, Patricia M. ; Sen, Sharmi ; Schneider‐Crease, India A. ; Chiou, Kenneth L. ; Lemma, Alemayehu ; Ayele, Ferehiwot ; Haile, Abebaw Azanaw ; Lu, Amy ; Bergman, Thore J. ; Beehner, Jacinta C. ; et al ( May 2023 , Molecular Ecology)

   Male reproductive competition can select for condition‐dependent, conspicuous traits that signal some aspect of fighting ability and facilitate assessment of potential rivals. However, the underlying mechanisms that link the signal to a male's current condition are difficult to investigate in wild populations, often requiring invasive experimental manipulation. Here, we use digital photographs and chest skin samples to investigate the mechanisms of a visual signal used in male competition in a wild primate, the red chest patch in geladas (Theropithecus gelada). We analysed photographs collected during natural (n = 144) and anaesthetized conditions (n = 38) to understand variability in male and female chest redness, and we used chest skin biopsies (n = 38) to explore sex differences in gene expression. Male and female geladas showed similar average redness, but males exhibited a wider within‐individual range in redness under natural conditions. These sex differences were also reflected at the molecular level, with 10.5% of genes exhibiting significant sex differences in expression. Subadult males exhibited intermediate gene expression patterns between adult males and females, pointing to mechanisms underlying the development of the red chest patch. We found that genes more highly expressed in males were associated with blood vessel development and maintenance but not with androgen or oestrogen activity. Together, our results suggest male gelada redness variability is driven by increased blood vessel branching in the chest skin, providing a potential link between male chest redness and current condition as increased blood circulation to exposed skin could lead to heat loss in the cold, high‐altitude environment of geladas.

    

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