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1. Transgressive hybrids as hopeful holobionts

   https://doi.org/10.1186/s40168-024-01994-8  

   Camper, Benjamin Thomas; Kanes, Andrew Stephen; Laughlin, Zachary Tyler; Manuel, Riley Tate; Bewick, Sharon Anne (January 2025, Microbiome)

   Abstract BackgroundHybridization between evolutionary lineages has profound impacts on the fitness and ecology of hybrid progeny. In extreme cases, the effects of hybridization can transcend ecological timescales by introducing trait novelty upon which evolution can act. Indeed, hybridization can even have macroevolutionary consequences, for example, as a driver of adaptive radiations and evolutionary innovations. Accordingly, hybridization is now recognized as a motor for macrobial evolution. By contrast, there has been substantially less progress made towards understanding the positive eco-evolutionary consequences of hybridization on holobionts. Rather, the emerging paradigm in holobiont literature is that hybridization disrupts symbiosis between a host lineage and its microbiome, leaving hybrids at a fitness deficit. These conclusions, however, have been drawn based on results from predominantly low-fitness hybrid organisms. Studying “dead-end” hybrids all but guarantees finding that hybridization is detrimental. This is the pitfall that Dobzhansky fell into over 80 years ago when he used hybrid sterility and inviability to conclude that hybridization hinders evolution. Goldschmidt, however, argued that rare saltational successes—so-called hopeful monsters—disproportionately drive positive evolutionary outcomes. Goldschmidt’s view is now becoming a widely accepted explanation for the prevalence of historical hybridization in extant macrobial lineages. Aligning holobiont research with this broader evolutionary perspective requires recognizing the importance of similar patterns in host–microbiome systems. That is, rare and successful “hopeful holobionts” (i.e., hopeful monsters at the holobiont scale) might be disproportionately responsible for holobiont evolution. If true, then it is these successful systems that we should be studying to assess impacts of hybridization on the macroevolutionary trajectories of host–microbiome symbioses. ResultsIn this paper, we explore the effects of hybridization on the gut (cloacal) and skin microbiota in an ecologically successful hybrid lizard,Aspidoscelis neomexicanus. Specifically, we test the hypothesis that hybrid lizards have host-associated (HA) microbiota traits strongly differentiated from their progenitor species. Across numerous hybrid microbiota phenotypes, we find widespread evidence of transgressive segregation. Further, microbiota restructuring broadly correlates with niche restructuring during hybridization. This suggests a relationship between HA microbiota traits and ecological success. ConclusionTransgressive segregation of HA microbiota traits is not only limited to hybrids at a fitness deficit but also occurs in ecologically successful hybrids. This suggests that hybridization may be a mechanism for generating novel and potentially beneficial holobiont phenotypes. Supporting such a conclusion, the correlations that we find between hybrid microbiota and the hybrid niche indicate that hybridization might change host microbiota in ways that promote a shift or an expansion in host niche space. If true, hybrid microbiota restructuring may underly ecological release from progenitors. This, in turn, could drive evolutionary diversification. Using our system as an example, we elaborate on the evolutionary implications of host hybridization within the context of holobiont theory and then outline the next steps for understanding the role of hybridization in holobiont research. 

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2. Within-species floral evolution reveals convergence in adaptive walks during incipient pollinator shift

   https://doi.org/10.1038/s41467-025-57639-3  

   Wenzell, Katherine_E; Neequaye, Mikhaela; Paajanen, Pirita; Hill, Lionel; Brett, Paul; Byers, Kelsey_J_R_P (March 2025, Nature Communications)

   Abstract Understanding how evolution proceeds from molecules to organisms to interactions requires integrative studies spanning biological levels. Linking phenotypes with associated genes and fitness illuminates how adaptive walks move organisms between fitness peaks. Floral evolution can confer rapid reproductive isolation, often converging in association with pollinator guilds. Within the monkeyflowers (Mimulussect.Erythranthe), yellow flowers within red hummingbird-pollinated species have arisen at least twice, suggesting possible pollinator shifts. We compare two yellow-flowered forms ofM. cardinalisandM. verbenaceusto their red counterparts in floral phenotypes, biochemistry, transcriptomic and genomic variation, and pollinator interactions. We find convergence in ongoing adaptive walks of both yellow morphs, with consistent changes in traits of large effect (floral pigments, associated gene expression), resulting in strong preference for yellow flowers by bumblebees. Shifts in scent emission and floral opening size also favor bee adaptation, suggesting smaller-effect steps from hummingbird to bee pollination. By examining intraspecific, incipient pollinator shifts in two related species, we elucidate adaptive walks at early stages, revealing how convergent large effect mutations (floral color) may drive pollinator attraction, followed by smaller effect changes for mechanical fit and reward access. Thus, ongoing adaptive walks may impact reproductive isolation and incipient speciation via convergent evolution. 

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3. 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. 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. 

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4. Spatiotemporal dynamics of genetic variation at the quantitative and molecular levels within a natural Arabidopsis thaliana population

   https://doi.org/10.1111/1365-2745.13981  

   Méndez‐Vigo, Belén; Castilla, Antonio R.; Gómez, Rocío; Marcer, Arnald; Alonso‐Blanco, Carlos; Picó, F. Xavier (November 2022, Journal of Ecology)

   Abstract Evolutionary change begins at the population scale. Therefore, understanding adaptive variation requires the identification of the factors maintaining and shaping standing genetic variation at the within‐population level. Spatial and temporal environmental heterogeneity represent ecological drivers of within‐population genetic variation, determining the evolutionary trajectory of populations along with random processes. Here, we focused on the effects of spatiotemporal heterogeneity on quantitative and molecular variation in a natural population of the annual plant Arabidopsis thaliana . We sampled 1093 individuals from a Spanish A. thaliana population across an area of 7.4 ha for 10 years (2012–2021). Based on a sample of 279 maternal lines, we estimated spatiotemporal variation in life‐history traits and fitness from a common garden experiment. We genotyped 884 individuals with nuclear microsatellites to estimate spatiotemporal variation in genetic diversity. We assessed spatial patterns by estimating spatial autocorrelation of traits and fine‐scale genetic structure. We analysed the relationships between phenotypic variation, geographical location and genetic relatedness, as well as the effects of environmental suitability and genetic rarity on phenotypic variation. The common garden experiment indicated that there was more temporal than spatial variation in life‐history traits and fitness. Despite the differences among years, genetic distance in ecologically relevant traits (e.g. flowering time) tended to be positively correlated to genetic distance among maternal lines, while isolation by distance was less important. Genetic diversity exhibited significant spatial structure at short distances, which were consistent among years. Finally, genetic rarity, and not environmental suitability, accounted for genetic variation in life‐history traits. Synthesis . Our study highlighted the importance of repeated sampling to detect the large amount of genetic diversity at the quantitative and molecular levels that a single A. thaliana population can harbour. Overall, population genetic attributes estimated from our long‐term monitoring scheme (genetic relatedness and genetic rarity), rather than biological (dispersal) or ecological (vegetation types and environmental suitability) factors, emerged as the most important drivers of within‐population structure of phenotypic variation in A. thaliana . 

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5. Ecological novelty at the start of the Cambrian and Ordovician radiations of echinoderms

   https://doi.org/10.1111/pala.12688  

   Novack‐Gottshall, Philip M.; Purcell, Jack; Sultan, Ali; Ranjha, Isa; Deline, Bradley; Sumrall, Colin D. (January 2024, Palaeontology)

   Abstract The Cambrian and Ordovician radiations marked the origins of all major echinoderm clades and established their Phanerozoic ecological blueprint. Recent claims of modest innovation of early echinoderms and other animals suggest constraints on novelty during the origins of phyla. Here, we document the life‐habit richness, body size, tiering, habitat usage, mobility, diet and foraging habits of 366 Cambrian–Ordovician echinoderm genera across a time‐scaled phylogeny to identify the timing and impact of novelty. Most early echinoderms were sedentary, filter‐feeding microbivores, and their body sizes, diets and modes of locomotion were largely unchanged through time, despite major volatility in taxonomic composition. Cambrian echinoderms lived close to the seafloor, with stylophorans first evolving semi‐infaunality. Many Ordovician echinoderms lived farther from the seafloor, with more complex filter‐feeding organs and tiering structure, often using other organisms as substrates. Mobile carnivores and mass‐feeders emerge then, too, across diverse asterozoans and echinozoans. Most of these novelties coincide with the origins of individual clades during the early and late Cambrian (Terreneuvian/Series 2 and Furongian), and 10–20 million years pass before most become ecologically important. Life‐habit evolution within most taxa involved new variations in these traits, with crinoids and asterozoans better able to shift strategies. The Ordovician radiation records more new variability in pre‐existing Cambrian life habits rather than radical re‐invention, with important novelties (like mobile carnivory and mass‐feeding, increased height off the seafloor, and biotic substrates) becoming ecologically more impactful. Taxa with these strategies were those best able to capitalize on the newly heterogeneous Ordovician world. 

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