Masakado Kawata

Sexual selection explains the evolution of exaggerated sexual displays, but less obvious is why biased mate preferences—a requirement for sexual selection—evolve. Fisher (1930) proposed that biased mate preferences can spark self-reinforcing evolutionary process (runaway) that drives their own evolution. This occurs because mate choice imposes sexual selection on sexual displays and links them genetically to mate preferences, producing indirect selection on the preferences themselves. While mathematical models have demonstrated the plausibility of the runaway theory, they rely on several idealized assumptions. Consequently, it remains poorly understood how runaway halts once populations deviate from these idealized conditions as a consequence of evolution via runaway, and how the genetic architecture underlying sexual displays influences the resulting evolutionary dynamics. Here, we address these gaps using two complementary approaches. First, we review and synthesize existing theories to classify the mechanisms that halt runaway into four categories, based on which idealized assumptions of Lande’s (1981) classic model are violated during evolution via runaway. Second, we conduct individual-based evolutionary simulations varying the genetic architecture of sexual displays from conventional additive to omnigenic inheritance models. Our results show that genetic architecture determines how runaway process halts, thereby governing long-term evolutionary dynamics under sexual selection.

Emotional vulnerability arises from the interplay of genetic variation, cortical network capacity, and subjective processing of adverse experiences, yet these components are rarely examined together in population-scale datasets. Monoaminergic signaling offers an opportunity for understanding such interactions because variation in related genes shapes sensitivity to environmental inputs. Among them, the vesicular monoamine transporter 1 ( VMAT1 ) Thr136Ile variant is notable for its functional effects and its long-term maintenance at intermediate frequencies, a pattern consistent with context-dependent selection. These properties make it an informative marker for investigating how genetic sensitivity interacts with neurobiological and experiential factors to shape affective functioning. Using data from up to 9,625 participants in the Tohoku Medical Megabank Project, a cohort established after the 2011 Great East Japan Earthquake, we investigated how monoaminergic variation, cortical morphology, and traumatic memory shape affective functioning. We found associations between the Thr136Ile variant and negative affectivity and depressive symptoms, consistent with prior reports of heightened emotional reactivity associated with the 136Thr allele. However, magnitude of these effects was substantially amplified in specific experiential and neurobiological contexts. Subjective trauma sensitivity, capturing the discrepancy between earthquake disruption and current traumatic memory, displayed a genotype-dependent association with depressive symptoms, and this relationship was strongest when parietal or insular cortical surface area was smaller. Together, these results identify a multilevel pathway through which monoaminergic variation contributes to emotional vulnerability by interacting with both cortical network capacity and trauma processing. The context-dependent influence of monoaminergic variation may further contribute to maintenance of affective diversity in human populations.

Short‐term responses to temperature stress, such as heat waves and long‐term acclimation to temperature changes, including seasonal shifts, are expected to be mediated by distinct molecular pathways. However, in ectotherms, such as reptiles, the effects of exposure duration on molecular responses to temperature change remain unclear. In this study, we investigated temperature‐induced molecular changes across distinct timescales in a newly established reptilian model species, the Madagascar ground gecko ( Paroedura picta ). To determine temperature‐responsive phenotypes and assess phenotypic plasticity under long‐term temperature changes, we compared thermal traits in individuals acclimated to 25°C and 30°C for more than 30 days. We found significant differences in the critical thermal minimum and maximum as well as sprint speed between the two groups. We then employed RNA sequencing and the assay for transposase‐accessible chromatin using sequencing to analyse gene expression, splicing and chromatin states across multiple temperature conditions and durations. Results revealed that abrupt temperature shifts activated known heat stress pathways, whereas prolonged temperature acclimation altered immune function. In the liver, the predicted occupancy of some transcription factors diverged between short‐ and long‐term temperature stimuli. These findings indicate that transient temperature stress responses and long‐term temperature acclimation in P. picta involve distinct molecular mechanisms.

Symbiosis is a basis for species diversification through interactions between organisms. In tropical and subtropical oceans, dinoflagellate symbionts belonging to the family Symbiodiniaceae, including the genus Symbiodinium, support the flourishment of cnidarian hosts, including corals, and thereby the ecology of oligotrophic oceans through their photosynthate carbon transfers. Although the genus Symbiodinium includes both free-living and symbiotic species, the detailed genetic background of their lifestyle differences remains unclear. In this study, we identified candidate genes involved in the evolutionary acquisition or maintenance of symbiosis in Symbiodinium spp. by detecting genes that have undergone positive selection during symbiotic and free-living lifestyle diversification. Using multiple Symbiodinium genomes to detect positive selection, 35 genes were identified, including a gene encoding soluble starch synthase SSY1 and genes related to metabolite secretion, which may be preferred for symbiotic lifestyles. In particular, our in silico analyses revealed that the SSY1 gene family has undergone extensive gene duplications in an ancestral dinoflagellate, and that the mutations detected as positive selection have occurred in the intrinsically disordered region of one of the homologs. Consistent with molecular evolution, the phenotypes of intracellular starch synthesis/accumulation were distinct between the symbiotic and free-living species of Symbiodinium when cultured under different pH and nitrogen conditions. These results provide molecular and phenotypic insights into symbiotic Symbiodinium-coral relationships.

Symbiosis is a basis for species diversification through interactions between organisms. In tropical and subtropical oceans, dinoflagellate symbionts belonging to the family Symbiodiniaceae, including the genus Symbiodinium , support the flourishment of cnidarian hosts, including corals, and thereby the ecology of oligotrophic oceans through their photosynthate carbon transfers. Although the genus Symbiodinium includes both free-living and symbiotic species, the detailed genetic background of their lifestyle differences remains unclear. In this study, we identified candidate genes involved in the evolutionary acquisition or maintenance of symbiosis in Symbiodinium spp. by detecting genes that have undergone positive selection during symbiotic and free-living lifestyle diversification. Using multiple Symbiodinium genomes to detect positive selection, 35 genes were identified, including a gene encoding soluble starch synthase SSY1 and genes related to metabolite secretion, which may be preferred for symbiotic lifestyles. In particular, our in silico analyses revealed that the SSY1 gene family has undergone extensive gene duplications in an ancestral dinoflagellate, and that the mutations detected as positive selection have occurred in the intrinsically disordered region of one of the homologs. Consistent with molecular evolution, the phenotypes of intracellular starch synthesis/accumulation were distinct between the symbiotic and free-living species of Symbiodinium when cultured under different pH and nitrogen conditions. These results provide molecular and phenotypic insights into symbiotic Symbiodinium -coral relationships. Significance statement: Clarifying how coral symbiont algae of the family Symbiodiniaceae are functionally diversified is crucial for understanding the molecular mechanisms of symbiotic relationships and interactions in animal-algal symbioses. However, gene-level molecular evolution that contributes to symbiotic relationships remains unclear. Our genome-wide single-gene analyses of the genus Symbiodinium , comprising both symbiotic and free-living species, successfully detected several dozen protein-coding genes that underwent symbiont-specific positive selection after divergence from the free-living species in the genus. Furthermore, our cultivation experiments demonstrated differences in photosynthate-related phenotypes between the symbiotic and free-living species. Our findings provide a key to illuminating the molecular evolution involved in phenotypic changes that potentially contribute to symbiotic lifestyles in Symbiodinium .

Understanding the genetic basis for adapting to thermal environments is important due to serious effects of global warming on ectothermic species. Various genes associated with thermal adaptation in lizards have been identified mainly focusing on changes in gene expression or the detection of positively selected genes using coding regions. Only a few comprehensive genome‐wide analyses have included noncoding regions. This study aimed to identify evolutionarily conserved and accelerated genomic regions using whole genomes of eight Anolis lizard species that have repeatedly adapted to similar thermal environments in multiple lineages. Evolutionarily conserved genomic regions were extracted as regions with overall sequence conservation (regions with fewer base substitutions) across all lineages compared with the neutral model. Genomic regions that underwent accelerated evolution in the lineage of interest were identified as those with more base substitutions in the target branch than in the entire background branch. Conserved elements across all branches were relatively abundant in “intergenic” genomic regions among noncoding regions. Accelerated regions (ARs) of each lineage contained a significantly greater proportion of noncoding RNA genes than the entire multiple alignment. Common genes containing ARs within 5 kb of their vicinity in lineages with similar thermal habitats were identified. Many genes associated with circadian rhythms and behavior were found in hot‐open and cool‐shaded habitat lineages. These genes might play a role in contributing to thermal adaptation and assist future studies examining the function of genes involved in thermal adaptation via genome editing.

Teleost fish exhibit remarkable sexual plasticity and divergent developmental systems, including sequential hermaphroditism. One of the more fascinating models of sexual plasticity is socially controlled sex change, which is often observed in coral reef fish. The Okinawa rubble goby, Trimma okinawae, is a bi-directional sex-changing fish. It can rapidly change sex in either direction based on social circumstances. Although behavioural and neuroendocrine sex change occurs immediately and is believed to trigger gonadal changes, the underlying mechanisms remain poorly understood. In this study, we conducted a de novo transcriptome analysis of the T. okinawae brain and identified genes that are differentially expressed between the sexes and genes that were immediately controlled by social stimulation implicating sex change. Several genes showed concordant expression shifts regardless of the sex change direction and were associated with histone modification in nerve cells. These genes are known to function in the neuroendocrine control of reproduction in nerve cells. Overall, we identified genes associated with the initiation of sex change, which provides insight into the regulation of sex change and sexual plasticity.

We examine the population genetic structure and divergence among the regional populations of the Japanese honeybee, Apis cerana japonica, by re‐sequencing the genomes of 105 individuals from the three main Japanese islands with diverse climates. The genetic structure results indicated that these individuals are distinct from the mainland Chinese A. cerana samples. Furthermore, population structure analyses have identified three genetically distinct geographic regions in Japan: Northern (Tohoku‐Kanto‐Chubu districts), Central (Chugoku district), and Southern (Kyushu district). In some districts, “possible non‐native” individuals, likely introduced from other regions in recent years, were discovered. Then, genome‐wide scans were conducted to detect candidate genes for adaptation by two different approaches. We performed a population branch statistics (PBS) analysis to identify candidate genes for population‐specific divergence. A latent factor mixed model (LFMM) was used to identify genes associated with climatic variables along a geographic gradient. The PBS_max analysis identified 25 candidate genes for population‐specific divergence whereas the LFMM analysis identified 73 candidate genes for adaptation to climatic variables along a geographic gradient. However, no common genes were identified by both methods.

Reef-building corals thrive in oligotrophic environments due to their possession of endosymbiotic algae. Confined to the low pH interior of the symbiosome within the cell, the algal symbiont provides the coral host with photosynthetically fixed carbon. However, it remains unknown how carbon is released from the algal symbiont for uptake by the host. Here we show, using cultured symbiotic dinoflagellate, Breviolum sp., that decreases in pH directly accelerates the release of monosaccharides, that is, glucose and galactose, into the ambient environment. Under low pH conditions, the cell surface structures were deformed and genes related to cellulase were significantly upregulated in Breviolum. Importantly, the release of monosaccharides was suppressed by the cellulase inhibitor, glucopyranoside, linking the release of carbon to degradation of the agal cell wall. Our results suggest that the low pH signals the cellulase-mediated release of monosaccharides from the algal cell wall as an environmental response in coral reef ecosystems.

Food intake is regulated by internal state. This function is mediated by hormones and neuropeptides, which are best characterized in popular model species. However, the evolutionary origins of such feeding-regulating neuropeptides are poorly understood. We used the jellyfishCladonemato address this question. Our combined transcriptomic, behavioral, and anatomical approaches identified GLWamide as a feeding-suppressing peptide that selectively inhibits tentacle contraction in this jellyfish. In the fruit flyDrosophila, myoinhibitory peptide (MIP) is a related satiety peptide. Surprisingly, we found that GLWamide and MIP were fully interchangeable in these evolutionarily distant species for feeding suppression. Our results suggest that the satiety signaling systems of diverse animals share an ancient origin.