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1. Recent reconfiguration of an ancient developmental gene regulatory network in Heliocidaris sea urchins

   Davidson, Phillip L ; Guo, Haobing ; Swart, Jane S ; Massri, Abdull J ; Edgar, Allison ; Wang, Lingyu ; Devens, Hannah R ; Koop, Demian ; Cisternas, Paula ; Zhang, He ; et al ( October 2022 , Nature ecology evolution)

   Changes in developmental gene regulatory networks (dGRNs) underlie much of the diversity of life, but the evolutionary mechanisms that operate on interactions with these networks remain poorly understood. Closely related species with extreme phenotypic divergence provide a valuable window into the genetic and molecular basis for changes in dGRNs and their relationship to adaptive changes in organismal traits. Here we analyze genomes, epigenomes, and transcriptomes during early development in two sea urchin species in the genus Heliocidaris that exhibit highly divergent life histories and in an outgroup species. Signatures of positive selection and changes in chromatin status within putative gene regulatory elements are both enriched on the branch leading to the derived life history, and particularly so near core dGRN genes; in contrast, positive selection within protein-coding regions have at most a modest enrichment in branch and function. Single-cell transcriptomes reveal a dramatic delay in cell fate specification in the derived state, which also has far fewer open chromatin regions, especially near dGRN genes with conserved roles in cell fate specification. Experimentally perturbing the function of three key transcription factors reveals profound evolutionary changes in the earliest events that pattern the embryo, disrupting regulatory interactions previously conserved for ~225 millionmore »years. Together, these results demonstrate that natural selection can rapidly reshape developmental gene expression on a broad scale when selective regimes abruptly change and that even highly conserved dGRNs and patterning mechanisms in the early embryo remain evolvable under appropriate ecological circumstances.« less
2. Trade-offs, Pleiotropy, and Shared Molecular Pathways: A Unified View of Constraints on Adaptation

   https://doi.org/10.1093/icb/icaa056  

   Mauro, Alexander A ; Ghalambor, Cameron K ( June 2020 , Integrative and Comparative Biology)

   Synopsis The concept of trade-offs permeates our thinking about adaptive evolution because they are exhibited at every level of biological organization, from molecular and cellular processes to organismal and ecological functions. Trade-offs inevitably arise because different traits do not occur in isolation, but instead are imbedded within complex, integrated systems that make up whole organisms. The genetic and mechanistic underpinning of trade-offs can be found in the pleiotropic nodes that occur in the biological pathways shared between traits. Yet, often trade-offs are only understood as statistical correlations, limiting the ability to evaluate the interplay between how selection and constraint interact during adaptive evolution. Here, we first review the classic paradigms in which physiologists and evolutionary biologists have studied trade-offs and highlight the ways in which network and molecular pathway approaches unify these paradigms. We discuss how these approaches allow researchers to evaluate why trade-offs arise and how selection can act to overcome trait correlations and evolutionary constraints. We argue that understanding how the conserved molecular pathways are shared between different traits and functions provides a conceptual framework for evolutionary biologists, physiologists, and molecular biologists to meaningfully work together toward the goal of understanding why correlations and trade-offs occur between traits.more »We briefly highlight the melanocortin system and the hormonal control of osmoregulation as two case studies where an understanding of shared molecular pathways reveals why trade-offs occur between seemingly unrelated traits. While we recognize that applying such approaches poses challenges and limitations particularly in the context of natural populations, we advocate for the view that focusing on the biological pathways responsible for trade-offs provides a unified conceptual context accessible to a broad range of integrative biologists.« less
3. Sexual selection and the ascent of women: Mate choice research since Darwin

   https://doi.org/10.1126/science.abi6308  

   Rosenthal, Gil G. ; Ryan, Michael J. ( January 2022 , Science)

   BACKGROUND Charles Darwin’s  Descent of Man, and Selection in Relation to Sex  tackled the two main controversies arising from the Origin of Species:  the evolution of humans from animal ancestors and the evolution of sexual ornaments. Most of the book focuses on the latter, Darwin’s theory of sexual selection. Research since supports his conjecture that songs, perfumes, and intricate dances evolve because they help secure mating partners. Evidence is overwhelming for a primary role of both male and female mate choice in sexual selection—not only through premating courtship but also through intimate interactions during and long after mating. But what makes one prospective mate more enticing than another? Darwin, shaped by misogyny and sexual prudery, invoked a “taste for the beautiful” without speculating on the origin of the “taste.” How to explain when the “final marriage ceremony” is between two rams? What of oral sex in bats, cloacal rubbing in bonobos, or the sexual spectrum in humans, all observable in Darwin’s time? By explaining desire through the lens of those male traits that caught his eyes and those of his gender and culture, Darwin elided these data in his theory of sexual evolution. Work since Darwin has focused on howmore »traits and preferences coevolve. Preferences can evolve even if attractive signals only predict offspring attractiveness, but most attention has gone to the intuitive but tenuous premise that mating with gorgeous partners yields vigorous offspring. By focusing on those aspects of mating preferences that coevolve with male traits, many of Darwin’s influential followers have followed the same narrow path. The sexual selection debate in the 1980s was framed as “good genes versus runaway”: Do preferences coevolve with traits because traits predict genetic benefits, or simply because they are beautiful? To the broader world this is still the conversation. ADVANCES Even as they evolve toward ever-more-beautiful signals and healthier offspring, mate-choice mechanisms and courter traits are locked in an arms race of coercion and resistance, persuasion and skepticism. Traits favored by sexual selection often do so at the expense of chooser fitness, creating sexual conflict. Choosers then evolve preferences in response to the costs imposed by courters. Often, though, the current traits of courters tell us little about how preferences arise. Sensory systems are often tuned to nonsexual cues like food, favoring mating signals resembling those cues. And preferences can emerge simply from selection on choosing conspecifics. Sexual selection can therefore arise from chooser biases that have nothing to do with ornaments. Choice may occur before mating, as Darwin emphasized, but individuals mate multiple times and bias fertilization and offspring care toward favored partners. Mate choice can thus occur in myriad ways after mating, through behavioral, morphological, and physiological mechanisms. Like other biological traits, mating preferences vary among individuals and species along multiple dimensions. Some of this is likely adaptive, as different individuals will have different optimal mates. Indeed, mate choice may be more about choosing compatible partners than picking the “best” mate in the absolute sense. Compatibility-based choice can drive or reinforce genetic divergence and lead to speciation. The mechanisms underlying the “taste for the beautiful” determine whether mate choice accelerates or inhibits reproductive isolation. If preferences are learned from parents, or covary with ecological differences like the sensory environment, then choice can promote genetic divergence. If everyone shares preferences for attractive ornaments, then choice promotes gene flow between lineages. OUTLOOK Two major trends continue to shift the emphasis away from male “beauty” and toward how and why individuals make sexual choices. The first integrates neuroscience, genomics, and physiology. We need not limit ourselves to the feathers and dances that dazzled Darwin, which gives us a vastly richer picture of mate choice. The second is that despite persistent structural inequities in academia, a broader range of people study a broader range of questions. This new focus confirms Darwin’s insight that mate choice makes a primary contribution to sexual selection, but suggests that sexual selection is often tangential to mate choice. This conclusion challenges a persistent belief with sinister roots, whereby mate choice is all about male ornaments. Under this view, females evolve to prefer handsome males who provide healthy offspring, or alternatively, to express flighty whims for arbitrary traits. But mate-choice mechanisms also evolve for a host of other reasons Understanding mate choice mechanisms is key to understanding how sexual decisions underlie speciation and adaptation to environmental change. New theory and technology allow us to explicitly connect decision-making mechanisms with their evolutionary consequences. A century and a half after Darwin, we can shift our focus to females and males as choosers, rather than the gaudy by-products of mate choice. Mate choice mechanisms across domains of life. Sensory periphery for stimulus detection (yellow), brain for perceptual integration and evaluation (orange), and reproductive structures for postmating choice among pollen or sperm (teal). ILLUSTRATION: KELLIE HOLOSKI/ SCIENCE« less
4. Transcriptomic and functional genetic evidence for distinct ecophysiological responses across complex life cycle stages

   https://doi.org/10.1242/jeb.244063  

   Freda, Philip J. ; Toxopeus, Jantina ; Dowle, Edwina J. ; Ali, Zainab M. ; Heter, Nicholas ; Collier, Rebekah L. ; Sower, Isaiah ; Tucker, Joseph C. ; Morgan, Theodore J. ; Ragland, Gregory J. ( June 2022 , Journal of Experimental Biology)

   ABSTRACT Organisms with complex life cycles demonstrate a remarkable ability to change their phenotypes across development, presumably as an evolutionary adaptation to developmentally variable environments. Developmental variation in environmentally sensitive performance, and thermal sensitivity in particular, has been well documented in holometabolous insects. For example, thermal performance in adults and juvenile stages exhibit little genetic correlation (genetic decoupling) and can evolve independently, resulting in divergent thermal responses. Yet, we understand very little about how this genetic decoupling occurs. We tested the hypothesis that genetic decoupling of thermal physiology is driven by fundamental differences in physiology between life stages, despite a potentially conserved cellular stress response. We used RNAseq to compare transcript expression in response to a cold stressor in Drosophila melanogaster larvae and adults and used RNA interference (RNAi) to test whether knocking down nine target genes differentially affected larval and adult cold tolerance. Transcriptomic responses of whole larvae and adults during and following exposure to −5°C were largely unique both in identity of responding transcripts and in temporal dynamics. Further, we analyzed the tissue-specificity of differentially expressed transcripts from FlyAtlas 2 data, and concluded that stage-specific differences in transcription were not simply driven by differences in tissue composition. Inmore »addition, RNAi of target genes resulted in largely stage-specific and sometimes sex-specific effects on cold tolerance. The combined evidence suggests that thermal physiology is largely stage-specific at the level of gene expression, and thus natural selection may be acting on different loci during the independent thermal adaptation of different life stages.« less
5. Behavioral variation, adaptation, and evolution

   https://doi.org/doi:10.1037/0000011-011  

   Shelton, D. S. ; Martins, E. P. ( January 2017 , APA)

   Individual animals behave differently from each other for myriad interrelated intrinsic and extrinsic reasons, and this behavioral variation is the raw substrate for evolutionary change. Behavioral varia- tion can both enhance and constrain long-term evolution (Foster, 2013), and it provides the basic materials on which natural and sexual selection can act. A rich body of historical experimental and conceptual foundations precedes many of the topics discussed. This classic literature is vast and impor- tant, and we encourage the reader to examine it in detail (e.g., Lehrman, 1953; Lorenz, 1971; Schnei- rla, 1966; Waddington, 1959) because we discuss more recent literature. For example, the study of the mechanisms that underlie behavioral variation has a divisive history, which involves carving out the relative contributions of genes and environment to a particular phenotype. Developmental systems and reaction-norm views challenged the issue of gene or environment by arguing that the interplay between genetic substrates and environmental inputs defined adaptive phenotypes across multiple contexts (Fos- ter, 2013; Gottlieb, 1991a, 1991b; Jablonka & Lamb, 2014). Identifying the interactional relationship between components permits researchers to under- stand how behavior becomes organized (Gottlieb, 1991a, 1991b) and can reveal links between indi- vidual variation and population-level persistence, species diversificationmore »(or stasis), and community dynamics (reviewed in Dingemanse & Wolf, 2013). Similarly, the study of individual differences has a rich history situated in the areas of behavioral genet- ics, sociobiology, behavioral ecology, developmen- tal psychology, personality theory, and studies of learning and cognition. Each area has its own goals, associated techniques, and levels of explanation. The study of behavioral variation during early develop- ment, for instance, has been documented primarily by psychologists studying proximate mechanisms in laboratory animal models, whereas the study of dif- ferent adult morphs using the adaptationist perspec- tive has been dominated by behavioral ecologists examining natural populations (Foster, 1995). A more complete description of individual differences requires an integrative study of the mechanisms (e.g., developmental, physiological) that guide intra- individual flexibility and the associated adaptive fine tuning of behavioral types. It is through this integra- tion that researchers can make predictions about the response of different individual phenotypes, groups, populations, and species to novel situations (e.g., captive and urban environments).« less