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1. 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 diversification (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). 

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2. Olfactory receptor gene evolution is unusually rapid across Tetrapoda and outpaces chemosensory phenotypic change

   https://doi.org/10.1093/cz/zoaa051  

   Yohe, Laurel R ; Fabbri, Matteo ; Hanson, Michael ; Bhullar, Bhart-Anjan S ( September 2020 , Current Zoology)

   Muñoz, Martha (Ed.)

   Abstract Chemosensation is the most ubiquitous sense in animals, enacted by the products of complex gene families that detect environmental chemical cues and larger-scale sensory structures that process these cues. While there is a general conception that olfactory receptor (OR) genes evolve rapidly, the universality of this phenomenon across vertebrates, and its magnitude, are unclear. The supposed correlation between molecular rates of chemosensory evolution and phenotypic diversity of chemosensory systems is largely untested. We combine comparative genomics and sensory morphology to test whether OR genes and olfactory phenotypic traits evolve at faster rates than other genes or traits. Using published genomes, we identified ORs in 21 tetrapods, including amphibians, reptiles, birds, and mammals and compared their rates of evolution to those of orthologous non-OR protein-coding genes. We found that, for all clades investigated, most OR genes evolve nearly an order of magnitude faster than other protein-coding genes, with many OR genes showing signatures of diversifying selection across nearly all taxa in this study. This rapid rate of evolution suggests that chemoreceptor genes are in “evolutionary overdrive,” perhaps evolving in response to the ever-changing chemical space of the environment. To obtain complementary morphological data, we stained whole fixed specimens with iodine, µCT-scanned the specimens, and digitally segmented chemosensory and nonchemosensory brain regions. We then estimated phenotypic variation within traits and among tetrapods. While we found considerable variation in chemosensory structures, they were no more diverse than nonchemosensory regions. We suggest chemoreceptor genes evolve quickly in reflection of an ever-changing chemical space, whereas chemosensory phenotypes and processing regions are more conserved because they use a standardized or constrained architecture to receive and process a range of chemical cues. 

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3. Proposing a neural framework for the evolution of elaborate courtship displays

   https://doi.org/10.7554/eLife.74860  

   Schwark, Ryan W ; Fuxjager, Matthew J ; Schmidt, Marc F ( May 2022 , eLife)

   In many vertebrates, courtship occurs through the performance of elaborate behavioral displays that are as spectacular as they are complex. The question of how sexual selection acts upon these animals’ neuromuscular systems to transform a repertoire of pre-existing movements into such remarkable (if not unusual) display routines has received relatively little research attention. This is a surprising gap in knowledge, given that unraveling this extraordinary process is central to understanding the evolution of behavioral diversity and its neural control. In many vertebrates, courtship displays often push the limits of neuromuscular performance, and often in a ritualized manner. These displays can range from songs that require rapid switching between two independently controlled ‘voice boxes’ to precisely choreographed acrobatics. Here, we propose a framework for thinking about how the brain might not only control these displays, but also shape their evolution. Our framework focuses specifically on a major midbrain area, which we view as a likely important node in the orchestration of the complex neural control of behavior used in the courtship process. This area is the periaqueductal grey (PAG), as studies suggest that it is both necessary and sufficient for the production of many instinctive survival behaviors, including courtship vocalizations. Thus, we speculate about why the PAG, as well as its key inputs, might serve as targets of sexual selection for display behavior. In doing so, we attempt to combine core ideas about the neural control of behavior with principles of display evolution. Our intent is to spur research in this area and bring together neurobiologists and behavioral ecologists to more fully understand the role that the brain might play in behavioral innovation and diversification. 

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4. 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 how 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 

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5. Variable Binding for Sparse Distributed Representations: Theory and Applications

   https://doi.org/10.1109/TNNLS.2021.3105949  

   Frady, Edward Paxon ; Kleyko, Denis ; Sommer, Friedrich T. ( September 2021 , IEEE Transactions on Neural Networks and Learning Systems)

   null (Ed.)

   Variable binding is a cornerstone of symbolic reasoning and cognition. But how binding can be implemented in connectionist models has puzzled neuroscientists, cognitive psychologists, and neural network researchers for many decades. One type of connectionist model that naturally includes a binding operation is vector symbolic architectures (VSAs). In contrast to other proposals for variable binding, the binding operation in VSAs is dimensionality-preserving, which enables representing complex hierarchical data structures, such as trees, while avoiding a combinatoric expansion of dimensionality. Classical VSAs encode symbols by dense randomized vectors, in which information is distributed throughout the entire neuron population. By contrast, in the brain, features are encoded more locally, by the activity of single neurons or small groups of neurons, often forming sparse vectors of neural activation. Following Laiho et al. (2015), we explore symbolic reasoning with a special case of sparse distributed representations. Using techniques from compressed sensing, we first show that variable binding in classical VSAs is mathematically equivalent to tensor product binding between sparse feature vectors, another well-known binding operation which increases dimensionality. This theoretical result motivates us to study two dimensionality-preserving binding methods that include a reduction of the tensor matrix into a single sparse vector. One binding method for general sparse vectors uses random projections, the other, block-local circular convolution, is defined for sparse vectors with block structure, sparse block-codes. Our experiments reveal that block-local circular convolution binding has ideal properties, whereas random projection based binding also works, but is lossy. We demonstrate in example applications that a VSA with block-local circular convolution and sparse block-codes reaches similar performance as classical VSAs. Finally, we discuss our results in the context of neuroscience and neural networks. 

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