Proceedings of the Royal Society B: Biological Sciences

Socially-controlled sex changing fishes provide powerful model systems for investigating sexual development and phenotypic plasticity in both behavior and physiology. The remarkable sexual transformation these fishes undertake is strongly influenced by their position in dominance hierarchies. However, the behavioral mechanisms underlying hierarchical formation remain understudied, particularly among female groups. Here, we investigated the role of winner-loser effects among females in establishing social dominance in a female-to-male sex changing fish. Individuals with prior losing experiences were more likely to lose subsequent size-matched fights, demonstrating clear loser effects, while there was no evidence for winner effects. Initial mirror aggression and some prior fighting behaviors, particularly submission, significantly and positively correlated with aggression in size-matched fights and subsequent mirror aggression; however, contest outcomes were not altered by these factors. Additionally, mirror aggression increased significantly only in subjects that drew size-matched fights. These findings demonstrate complex fighting dynamics in female-female competition and confirm the presence of loser effects in a sequential hermaphroditic species. These effects may represent evolutionarily advantageous mechanisms underlying sex change, thereby offering further context for examining how social rank advantages drive sexual transition.

Vector-borne pathogens cause 17% of all human infectious diseases, and rising global temperatures are shifting the distribution and abundance of mosquito vectors. Because mosquitoes are ectotherms, temperature strongly governs biological rates and physiology; however, mosquitoes also experience other environmental factors that may interact with temperature to shape the thermal performance of traits driving population dynamics. Here, we use a factorial life-table experiment spanning five relative humidities (30-90%) and seven temperatures (16-38{whitebullet}C) to show that humidity modifies the thermal performance of key fitness traits in adult Anopheles stephensi, an invasive urban malaria vector. When integrated into a demographic model, humidity markedly reshapes projections of population fitness relative to temperatureonly models, suppressing growth and contracting year-round suitability in hot, arid regions while enhancing fitness in more humid or high-elevation climates characteristic of South Asia and Africa. Together, these results highlight the need to integrate multiple environmental drivers into projections of climatic suitability, as temperature-only approaches may mischaracterize both the magnitude and spatial structure of mosquito population fitness. More broadly, our findings demonstrate how moisture availability reshapes thermal niches, population fitness, and climate-driven projections of vector distributions.

Collective behavior in animal societies can buffer individual costs and confer resilience to environmental challenges. However, the mechanisms by which groups sustain function when members are compromised remain poorly understood. In the presented study, we investigate how social context shapes collective fanning, a thermoregulatory behavior critical for colony function, in Western honeybees (Apis mellifera). Using oxytetracycline (OTC), a known physiologically disruptive antibiotic to honeybees, to selectively impair certain group members, we tested our hypothesis that the presence of untreated bees would rescue the fanning response in mixed-composition groups. We show that groups containing untreated individuals fan at levels comparable to fully untreated groups, despite the presence of OTC-impaired bees. This preservation of collective thermoregulatory function was correlated with both treated and untreated individuals in mixed groups shifting their interaction dynamics and social network positions. These findings reveal a decentralized mechanism of collective resilience, whereby behavioral compensation by individuals sustains group-level thermoregulation under partial disruption. Our results provide a framework for understanding how social insect colonies maintain function in the face of individual-level perturbations, with broader implications for predicting the limits of collective resilience in animal societies experiencing increasing environmental pressures.

Eusocial insects fascinate researchers with their sophisticated communication systems and sensory specialisations. Ants and termites have coexisted in a long-standing predator-prey arms race, offering insight into the interplay between ecology and evolution. The subterranean termite Coptotermes acinaciformis can detect the predatory ant Iridomyrmex purpureus through footstep-induced vibrations, triggering defensive responses. Ants produce noisier walking signatures than termites, while the inquiline termite Macrognathotermes sunteri walks more quietly than its host, suggesting species-specific vibroacoustic strategies. Using statistical analysis of video-tracked motion and footstep vibrations in confined arenas across six ant and ten termite species, we show that C. acinaciformis, despite its body size, moves more smoothly than ants, which alternate between directed and erratic paths. Inquiline termites, by contrast, displayed erratic movements. Ants consistently produced stronger vibrations closely linked to body mass, while Highly Comparative Time Series Analysis revealed termite motions approaching chaotic dynamics. Notably, while C. acinaciformis and I. purpureus produced distinct vibrational signatures, M. sunteri s signals overlapped with its host, consistent with vibroacoustic mimicry. Although the ecological nature of this association remains unresolved, our findings underscore the central role of vibrational cues in shaping interspecific dynamics and highlight vibroacoustic communication as an underappreciated driver of social insect ecology and evolution.

Phenotypic diversity is often thought to arise from the evolutionary modification of developmental processes. However, developmental processes are tightly coupled in space and time, with each process beginning from conditions set by the one before it. While we know from dynamical systems theory that initial conditions can significantly affect a systems out-come, their importance as a source of phenotypic evolvability has been largely overlooked. Here we show for the first time, that phenotypic evolution can proceed through changes in developmental initial conditions while the underlying developmental process remains conserved. Somitogenesis is the process by which vertebral precursors, known as somites, are periodically patterned in the pre-somitic mesoderm (PSM). Somitic count (total number of somites) is thought to diversify through the evolution of components of somitogenesis such as the tempo of the segmentation clock or the mechanisms driving axial morphogenesis. Using two closely related species of Lake Malawi cichlid fishes that differ in vertebral counts, we show that somite count evolution has happened without changes to somitogenesis itself, but instead, by altering the size of the PSM at the onset of this process. This work will expand what we consider developmental drivers of phenotypic evolution and highlight the importance of comparative studies to understand the diversification of phenotypes.

Usutu virus (USUV) is a mosquito-borne flavivirus that has recently expanded northwards in Europe and become endemic in the UK [1-3]. USUV emergence often precedes the closely related West Nile virus (WNV), potentially reflecting differences in epidemiological parameters [4, 5]. One key parameter is the extrinsic incubation period (EIP), the time required for a mosquito to become infectious following an infected blood meal. Here we present the first ever estimate of the temperature-dependent EIP for USUV in the vector Culex pipiens molestus. We were able to quantify the shortening of the EIP with temperature by re-analysing published laboratory data with bespoke Bayesian model that accounted for key features of the experimental design. Under typical UK summer temperatures, the median EIP (EIP50) of USUV is shorter than that of WNV, and the potential transmission season of USUV is both longer and geographically more extensive. Under RCP8.5 climate projections, WNV transmission suitability is expected to match or exceed current USUV levels between 2055 and 2065, highlighting the future threat to the UK from emerging mosquito-borne pathogens. Our findings support USUV as a precursor for WNV in northern Europe and provide a robust characterisation of a key epidemiological parameter of USUV, enabling accurate modelling of its transmission dynamics.

Research on stochastic phenotypic variation (i.e., variation arising despite the apparent absence of genetic and environmental differences) has recently emerged as a rapidly growing area in biological research. But despite growing recognition of both its existence and fitness relevance, it remains unknown whether and to what extent such stochastically induced variation is transmitted across generations, potentially making it an unrecognized contributor to evolutionary processes and the adaptive potential of populations. In order to address this knowledge gap, we here performed a two-generation behavioral screening with a naturally clonal fish: 34 genetically identical mothers and their 232 offspring were separated directly after birth into near-identical environments and tracked continuously at high resolution, constituting a total of [~]19,000 observation hours. We find that consistent among-individual differences in behavioral profiles (i.e., activity and feeding patterns) of both mothers and offspring emerged despite the absence of apparent genetic and environmental differences. Mother feeding behavior - but not mother activity - was positively associated with offspring activity: mothers that spent more time feeding produced more active offspring, explaining [~] 33 % of the total variation in offspring activity. This link between mother and offspring behavior was not mediated by mother size or offspring size at parturition. Our study provides first evidence for the non-genetic transmission of among-individual phenotypic differences that arise despite the apparent lack of genetic or environmental variation, highlighting the potential importance of this variation for evolutionary processes and the adaptability of populations.

In the search for universals shaping acoustic communication across species, we increasingly look for patterns known from human languages and music in non-human animals. These parallels are often explored separately and with limited ecological context. Here, we take a deep dive into the temporal structure of a complex call used by the little auk (Alle alle), a pelagic seabird with elaborate vocal behaviour and socially complex colonial life. Based on syllable durations, intervals and silences, we examine its conformance to linguistic laws, rhythmic structure and information content. This reveals intricate problems of temporal organisation: while the calls conform not only to linguistic laws of brevity but also to the initial and final lengthening known from human prosody, these effects interact with the internal structure of the call and information carried within it. To our knowledge, this is the first time that conformance to multiple linguistic laws, exceeding simple vocal efficiency, has been described for a non-human, non-vocal learning animal. The calls rhythmic structure shows a progressive rallentando -- a systematic slowing driven by changes in syllable and silence durations and the intervals between syllable onsets. The exact patterns of this rallentando are indicative of the callers sex and individually specific. These results reveal how seabird communication is shaped not only by efficiency universals, but also the specific pressures of colonial life. Our work highlights the temporal structure as an important axis of communication evolution, but also serves as a reminder to consider the species ecological reality and the function, not only presence, of temporal organisation. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=127 SRC="FIGDIR/small/713940v1_ufig1.gif" ALT="Figure 1"> View larger version (38K): org.highwire.dtl.DTLVardef@13de3a8org.highwire.dtl.DTLVardef@2d64adorg.highwire.dtl.DTLVardef@2ca53aorg.highwire.dtl.DTLVardef@113c38d_HPS_FORMAT_FIGEXP M_FIG C_FIG

Biotic interactions can drive evolutionary diversification, but the underlying mechanisms differ depending on the type of interaction. For instance, Ehrlich and Ravens escape-and-radiate coevolution provides a pathway of diversification in antagonistic interactions, whereas in mutualistic networks, coevolution is hypothesized to result in trait convergence rather than diversification. The combined effect of mutualism and antagonism on diversification remains unclear, even though organisms naturally engage in multiple types of interactions simultaneously. Using an eco-evolutionary simulation model, we investigate diversification in tripartite ecological networks such as plant-pollinator-herbivore networks. We find that diversification patterns vary according to the way mutualism and antagonism are connected on the trait level. If the two interactions are governed by uncorrelated plant traits, we observe little diversification in the mutualistic and substantial diversification in the antagonistic subnetwork. By contrast, if the same plant trait mediates both mutualism and antagonism (an example of ecological pleiotropy), diversification rates in all guilds become interdependent. In this case, even the mutualistic guild diversifies considerably when antagonism is strong, while strong mutualism restricts diversification also in the antagonistic guild. Our study underlines that the inclusion of multiple interaction types is necessary to advance our understanding of evolutionary dynamics in ecological networks.

O_LIPhenological shifts are a major ecological consequence of climate change, yet studies often focus on single life stages meaning that the potential for carryover effects between life stages remains poorly understood. Failing to account for these effects may lead to inaccurate estimates of phenological shifts, with consequences for predicted synchrony among interacting species. This is especially relevant for temperate systems where climate warming is occurring unevenly across the year. C_LIO_LIHere, we investigated how temperature experienced the previous autumn and winter (during the pupal and egg stage) influences spring phenology in the winter moth (Operophtera brumata), a herbivorous insect with distinct life stages. Using 50 years of local climate data to create five experimental temperature regimes, we first quantified phenotypic plasticity in the duration and temporal variability of pupal and egg development. We then examined how timing of adult moth emergence affects timing of offspring hatching. C_LIO_LIWe found divergent effects of temperature on different life stages; pupal development time was shortest at intermediate temperatures while egg development time decreased linearly with increasing temperature. Furthermore, phenological shifts due to the conditions experienced by the mother were carried over to influence the phenology of her offspring. While this carryover effect was partially compensated during subsequent stages, compensation decreased under warming conditions. C_LIO_LIThese results refine our understanding of the sensitivity of the annual cycle of winter moth phenology to variation in temperature with potential implications for population dynamics and interspecific interactions. Overall, our findings highlight the need to consider the impacts of warming across multiple life stages so that carryover effects can be properly accounted for. Doing so will improve predictions of phenological shifts under future climates. C_LI

O_LISeasonal patterns of species appearances constitute a major component of diversity variation. Theory attributes this phenological structuring of communities to the alignment of life cycles to suitable moments and to constraints of seasonality on development, yet the specific mechanisms operating across taxa remain largely unresolved. In insects, body size and colour are key functional traits that contribute to driving spatial community assembly through their link to thermoregulatory performance and development. C_LIO_LIHere we analyse variation in mean body size and colour lightness of 483 butterfly assemblages across Great Britain and throughout the season to test whether trait alignment with seasonal environment and developmental constraints may shape the phenological structuring of communities. C_LIO_LIBoth body size and body colour varied more along season than across space, emphasizing the importance of phenology on diversity variation. Body size was larger early and late in the season, i.e. under conditions of low temperature and solar radiation. This pattern contrasted with the spatial trends found and was driven by species overwintering as adults, which we interpret as being likely due to energetic constraints. Body colour, conversely, was darker early and late in the season, mirroring the spatial pattern found, and suggesting a thermoregulatory alignment with seasonal conditions. Furthermore, covariation between body size and colour suggests a thermoregulatory interaction between both traits. C_LIO_LIOur findings suggest that life-cycle constraints and seasonal thermoregulatory alignment contribute to shaping the phenological structure of insect communities. C_LI

Conspicuous coloration in animals is generally thought to evolve and be maintained through inter- or intraspecific interactions such as mate choice, but this might not always be the case. The sight-line hypothesis proposes that conspicuous light-dark contrast in front of the eyes (hereafter, eyeline) evolves and is maintained due to viability selection, enhancing an individual visual acuity and thus evolutionarily associated with a particular foraging behavior that requires accurate aiming. However, empirical evidence that supports the sight-line hypothesis is virtually absent, with no studies demonstrating the key prediction that the direction of eyelines matters. Here, I tested the sight-line hypothesis using macroevolutionary analyses in terns and allies, which are a suitable study system, because they have variation in facial color patterns, including presence/absence and, if any, various angles of eyelines. They also have a large variation in foraging behavior, including picking, plunge diving, and skimming. As predicted by the sight-line hypothesis, tern lineages that require accurate aiming at foraging (e.g., plunge diving) are more likely to have eyelines. In addition, the evolutionary transition to the state with eyelines and these foraging behaviors was more likely to occur than the reverse transition. Furthermore, as expected by the fact that the direction of travel is upwardly deviated from the direction of the bills during skimming, the eyeline angle from bills was evolutionarily positively associated with the occurrence of skimming behavior. To my knowledge, the current study is the first to demonstrate that the direction of the eyeline matters, thereby strongly supporting the sight-line hypothesis.

Collective decision-making in animal groups is often studied using short, trial-based mazes experimental setups that restrict observations to isolated choice events. However, how leadership and decision dynamics unfold over extended periods in symmetric environments remains poorly understood. Here we introduce a novel cyclic three-room Y-shaped environment that enables continuous, and autonomous sequences of collective decisions without experimental reset. We tracked the positions and identities of 20 groups of five AB-strand zebrafish (Danio rerio) during one-hour sessions in which animals freely transitioned between three identical rooms connected by visually isolated identical corridors. We show that this symmetric Y-maze enables the collection of large amounts of data to study decision-making with a few replicates, because habituation occurs after 45 minutes of exploration. After an initial exploration phase, groups reached a stable behavioural regime, generating thousands of decision events per replicate. Collective dynamics were consistent across spatial contexts, indicating that the symmetric architecture does not bias movement patterns, as opposed to traditional mazes. We show that zebrafish leadership is typically shared among shoal members, with leaders often acting as decision-makers. By transforming a classical maze into a self-renewing decision system, this approach enables the study of long-term collective dynamics and spontaneous leadership in controlled yet ecologically relevant conditions. Author summarypresentation

Vocal accommodation is the process by which individuals adjust their vocalizations to resemble those of social partners. This phenomenon is widespread in social animals and can reinforce affiliation, signal group identity, and facilitate coordination. Most studies of vocal accommodation have focused on convergence in the acoustic structure of individual calls. Whether social partners also converge in how calls are arranged into sequences remains largely unknown. We examined vocal convergence during pair formation in common marmosets (Callithrix jacchus) by recording phee sequences from nine dyads composed of three males and three females before pairing and again four months after, in two audience contexts: when individuals interacted vocally with their partner or with an opposite sex stranger. We quantified similarity between individuals in call sequence-structure using transition probabilities, bigram frequencies, repeat-length distributions, and local alignment, and quantified similarity in acoustic structure using spectral parameters, MFCCs, and dynamic time warping. We found vocal convergence on a sequence level. After pair formation, partners became more similar in sequence structure when calling to strangers, whereas no change was detected in partner directed sequences. In contrast, call acoustic structure did not change in either context. Because vocal repertoires are constrained by anatomy and physiology, reorganizing existing call types into different combinations may provide a flexible route for modifying signals without altering the acoustic structure of individual calls. Our results provide evidence that social bonds can drive sequence level vocal convergence in a non-human primate, suggesting that vocal flexibility may arise not only through changes in acoustic structures but also through changes in how calls are organized over time.

Resource availability is a central driver of ecological and evolutionary processes, yet its effects on infectious disease and virulence are not fully understood. A key limitation is that many studies consider only a narrow range of resource conditions or a limited subset of host and pathogen traits, potentially obscuring non-linear relationships. Here, we quantify how a gradient of six food levels simultaneously shapes host fitness and pathogen performance in the Daphnia magna- Ordospora colligata system. Across two laboratory experiments, we measured infection rates, pathogen burden, host fecundity, survival, and filtration rates. Increased food availability enhanced pathogen fitness, with both infection rates and spore burden increasing with provisioning. In contrast, host responses were trait-specific: while fecundity increased with food availability, pathogen-induced reductions in fecundity (i.e., virulence) peaked at intermediate resource levels, despite continued increases in pathogen load. This pattern indicates that resource availability alters host tolerance as well as pathogen growth, generating non-linear disease outcomes. Host survival was unaffected by either food provisioning or infection, further demonstrating that resource availability can simultaneously influence host and pathogen traits in different directions. Our results highlight the importance of integrating multiple fitness components across provisioning levels to understand disease dynamics and suggest that ongoing anthropogenic changes in resource availability may alter host-pathogen interactions.

Interactions among co-circulating parasite species influence infection risk and disease progression. Such interactions can occur within hosts, for example altering susceptibility, or indirectly through host demography or movement, potentially affecting landscape-scale transmission. Despite their ubiquity, the spatial implications of these interactions have received limited attention. We combine spatially-explicit modelling with laboratory experiments to investigate how different parasite-parasite interactions influence disease spread. We model within-host, demographic, and dispersal-related interactions across a linear landscape, showing that within-host interactions modifying host susceptibility have the strongest effects on parasite prevalence, spatial heterogeneity, and rate of spread. Furthermore, these effects are amplified when parasites invade sequentially, generating pronounced patch-level spatial priority effects. We tested these predictions experimentally using a protist host (Paramecium caudatum) and two bacterial parasites (Holospora undulata and H. obtusa). Consistent with model predictions, we found that H. obtusa reduces prevalence and spatial spread of H. undulata through reductions in host susceptibility, and found evidence for spatial priority effects, observing reduced H. undulata prevalence when introduced after H. obtusa. Our theoretical and experimental results highlight that parasite-parasite interactions can have important implications for parasite spatial epidemiology, but the magnitude of those effects depend on the interaction type and the timing of invasion.

Protogynous sex change, where individuals first function as females and later as males, is a key life-history strategy among polygynous reef fishes. In haremic systems, sex change is typically socially regulated, with dominants suppressing subordinates sex change through aggression. Females within a harem form a size-based hierarchy that can remain stable in most species through the threat of eviction. We studied a different situation in the cleaner wrasse Labroides dimidiatus, where larger females have incomplete control, as they spend most of their time alone at their own cleaning territory. We tracked over 400 individuals for 12 months, recording growth, behavior, social organization, and sex change. We confirmed earlier reports that both sexes direct aggression primarily at those ranked immediately below them. However, we observed 30 cases where smaller females outgrew larger ones, revealing hierarchy instability. Of 42 sex change events, 43% occurred in presence of the male, and half of these early sex changers were not the largest female, but individuals overlooked by the male. Fast growth relative to harem-mates and harem switching increased the likelihood of sex change. Local population densities also influenced growth and sex change, with individuals in high-density demes growing faster and changing sex at larger sizes. Our findings reveal flexible sex change dynamics in a system with incomplete social dominance. Such incomplete control and observations that becoming male confers both higher reproductive success and survival highlight the need to expand game-theoretical and life-history frameworks to encompass such strategic flexibility. Lay summaryDominant cleaner wrasse cannot fully control subordinates as individuals occupy distinct core areas. Tracking 400 fish for a year, we found that smaller females could outgrow initially larger ones, and early sex change despite a larger male. Fast growth and harem switching increased the chances of becoming male. Population density also shaped these strategies. Our findings reveal flexible sex change dynamics in a system where becoming male confers both higher reproductive success and survival.

Population genetic models excel at identifying the conditions for polymorphisms based on balancing selection but typically disregard the ecological processes that yield particular values of selection coefficients. We model a system that combines antagonistic pleiotropy, dominance reversal and heterozygote advantage: the wood tiger moth Arctia plantaginis, where alternative haplotypes at a major-effect locus determine male hindwing coloration. Yellow offers better protection against predators, while white is often associated with better mating success. The effects of mortality and reproductive success overlap in time because protandrous males can mate as long as they are alive, but they need to avoid predation for several days before the bulk of females emerge. We show that protandry aids polymorphism maintenance whenever the second-fittest genotype (after the heterozygote) is the poorly surviving but mating advantaged homozygote, while increased protandry harms polymorphism when the second-best fitness is that of the survival advantaged morph. Ecologically plausible protandry times predict that dominance reversal does not have to be strong for polymorphism to be maintained. Our study highlights the importance of timing traits in maintaining polymorphisms in Lepidoptera and showcases the benefits of deriving fitness explicitly in place of abstract selection coefficients that lack temporal components within the life cycle.

Understanding the distribution of paternity within social groups is critical for testing hypotheses about the evolution of behavior and morphology in primates, but assembling the requisite comparative data is a challenging task. We compiled genetic paternity data from 52 species of wild nonhuman primates along with information about socioecological, morphological, and life history traits that are relevant to understanding what proportion of offspring are sired by primary males (i.e., alpha males in multi-male groups and resident males in single male groups). Our dataset, which currently contains information about 11 primate families and >3,000 individual paternities, is presented as a publicly accessible, living database designed to be updated as new data become available. Using Bayesian regression models, we investigated the role that phylogeny, group composition, and seasonality play in determining primary males paternity share, and assessed the relative share of paternities obtained by non-primary residents versus extra-group males. First, we found that phylogeny has a detectable but relatively modest influence on primary males paternity share. Species-level differences explained roughly 35-40% of variation in primary males paternity share, and of that interspecific variation, [~]50-70% was attributable to shared phylogenetic history. Second, group composition strongly predicted paternity share outcomes. Primary males in single-male/multi-female groups obtained the highest share of paternity ([~]80%), while those in multi-male groups had the lowest ([~]60%), though there was substantial variation within each category. Pair-living animals showed a striking split: males in cohesive pairs sired [~]90% of offspring, while those in dispersed pairs sired only [~]55%. Contrary to expectations, reproductive seasonality did not predict primary males paternity share in any group type. Finally, when primary males in multi-male groups lost paternities, [~]75% of losses were to other resident males. Overall, [~]5-15% of offspring in these groups were sired by extra-group males. Our results largely confirm earlier findings based on smaller datasets, but also show that the relationship between social organization and paternity is more complicated than simple categorical predictions suggest. We discuss the gap between the data that would ideally be available for testing these hypotheses versus what currently exists, with hopes that our living database can help close this gap over time.

2The genotype-to-phenotype architecture (GPA), defined by complex interactions such as pleiotropy, epistasis, and regulatory control, is a fundamental yet often overlooked driver of biodiversity dynamics. While empirical evidence suggests that traits mediating species interactions (biotic) and environmental responses (abiotic) are frequently correlated, most eco-evolutionary theories treat these traits as independent, leaving a gap in our understanding of how genomic architecture influences community-level outcomes. In this study, we contrast two distinct GPAs, modular (independent trait evolution) and correlated (integrated trait evolution), within a spatially explicit multilayer network framework. We evaluate their impact on biodiversity across varying regimes of selection, migration, and biotic and environmental filtering. Our results reveal a hierarchy of drivers: selection strength dictates the absolute magnitude of the architectural effect, while migration and context-dependent biotic and abiotic effects determine which architecture yields a diversity advantage. Correlated GPAs enhance species coexistence and diversity in low-migration landscapes characterized by strong selection and moderate, balanced biotic and abiotic pressures. In these contexts, trait integration serves as a buffer against selective noise. Conversely, modular GPAs support higher diversity under high migration and strong biotic interactions, where the decoupling of trait modules provides the adaptive flexibility necessary to navigate spatially conflicting selective pressures. Our findings demonstrate that genomic architecture acts as a critical filter for environmental perturbations. Integrating complex GPAs into multispecies models is essential for quantifying the co-evolutionary feedbacks among traits, population adaptation, and species persistence. Our framework provides a path for predicting how biodiversity emerges and persists across biological scales, from genomics to communities and food webs, under the accelerating pressures of global change. 1 ConclusionsO_LIWe integrate trait architecture to spatial biodiversity to show biodiversity patterns are not merely products of ecological interactions, but are fundamentally constrained by Genotype-to-Phenotype Architecture (GPA). By linking GPA to biodiversity we show the interplay between the complexity of an organism and community structure in determining diversity patterns. C_LIO_LIThe hierarchy of Eco-Evolutionary Drivers: We establish a new conceptual hierarchy where selection strength acts as the fundamental governor of architectural impact, while the specific architecture predicting higher diversity (Correlational vs. Modular) is dictated by the interplay of migration scales and context-dependent biotic and abiotic dynamics. C_LIO_LISelection-Migration contingency for coexistence: We provide a new hypothesis for species coexistence: Correlational selection serves as a stabilizing force under dispersal limitation, whereas Modular trait architecture provides the adaptive flexibility to maintain diversity in high-migration, spatially heterogeneous landscapes. C_LIO_LIAdaptive decoupling as a diversity engine: We propose that trait modularity functions as a "buffer" against extinction by decoupling phenotypic responses. This allows populations to navigate conflicting selective pressures, effectively facilitating evolutionary rescue in complex biotic environments. C_LIO_LIMethodological framework for empirical inference: To bridge the gap between theory and data, we provide a novel likelihood-based framework. This enables researchers to infer latent trait architectures from population genomic samplings, turning GPA from a theoretical construct into a measurable sampling variable in natural populations. C_LIO_LIWe define a new roadmap for the next generation of eco-evolutionary modeling. By identifying the gaps between existing simulation engines, we provide a conceptual "blueprint" for a digital ecosystem that fully integrates complex genetic architecture with global bio-diversity dynamics. C_LI