The evolution of reproductive leaf dimorphism in two globally distributed fern families is neither stepwise nor irreversible, unless further specialization evolves.

A contemporary interpretation of Dollo's Law is that the evolution of specialized structures is irreversible. Among land plants, reproductive specialization shows a trend toward increasing complexity without reversion, raising questions about evolutionary steps and irreversibility of reproductive complexity. Ferns, exhibit varied reproductive strategies, some are dimorphic (producing separate leaves for photosynthesis and reproduction), while others are monomorphic (where one leaf is used for both photosynthesis and spore dispersal). This diversity provides an opportunity to examine the applicability of Dollo's Law in the evolution of reproductive leaf specialization across plants. We analyzed 118 species in Blechnaceae and Onocleaceae using quantitative morphometrics and phylogenetic comparative methods to test the pillars of Dollo's Law of irreversibility. The evolution of dimorphism in Blechnaceae is neither stepwise nor irreversible, with direct transitions from monomorphism to dimorphism, including several reversions. In contrast, Onocleaceae exhibit irreversibility to monomorphism upon further specialization of fertile leaves for spore dispersal, suggesting that additional specialization, not dimorphism alone, may facilitate irreversibility. These results provide insight into the canalization of fertile-sterile leaf dimorphism in seed plants, where traits like heterospory and ovules lead to further specialization and potential irreversibility. These findings suggest that as new specialized traits evolve alongside pre-existing ones, reversion may become increasingly unlikely.

Expansion of MHC-IIB has constrained the evolution of MHC-IIA in passerines.

The major histocompatibility complex (MHC) is central in adaptive immunity, with the highly polymorphic MHC genes encoding antigen-presenting molecules. Two MHC class II (MHC-II) loci, DA1 and DA2, pre-date the radiation of extant birds and persist throughout much of the avian phylogeny. Within each locus, the MHC-II molecules are encoded by A- (DAA) and B- (DAB) genes, which are arranged in A-B dyads. However, in passerines (order Passeriformes), the DA2 locus has been lost and the ancestral A-B dyad at the DA1 locus has been replaced by a putatively single A-gene (DAA1) and an array of highly polymorphic B-genes (DAB1). In this study, we genotyped the DAA1 gene of 15 passerine species and confirmed that passerines possess just one copy of DAA1. We then compared selection patterns in DAA1 between passerines and non-passerines and found that exon 2, which encodes the antigen-presenting domain, has been subject to weaker positive selection and stronger negative selection in passerines compared with non-passerines. Additional comparisons showed that the patterns of selection in the passerine DAA1 gene are unlikely to be related to the loss of the DA2 locus. Instead, our findings suggest that the expansion of DAB1 (MHC-IIB) has imposed an evolutionary constraint on the passerine DAA1 (MHC-IIA) gene. We speculate that this constraint may be the result of each DAA1 chain having to form heterodimers with many different DAB1 chains.

The case against simplistic genetic explanations of evolution.

Humans are curious to understand the causes of traits that distinguish us from other animals and that distinguish vastly different species from one another. We also have a proclivity for simple stories and sometimes tend toward seeking and accepting simple genetic explanations for large evolutionary shifts, even to a single gene. Here, I reveal how a biased expectation of mechanistic simplicity threads through the long history of evolutionary and developmental genetics. I argue, however, that expecting a simple mechanism threatens a deeper understanding of evolution, and I define the limitations for interpreting experimental evidence in evolutionary developmental genetics.

Skull sinuses precluded extinct crocodile relatives from cetacean-style deep diving as they transitioned from land to sea.

During major evolutionary transitions, groups develop radically new body plans and radiate into new habitats. A classic example is cetaceans which evolved from terrestrial ancestors to become pelagic swimmers. In doing so, they altered their air-filled sinuses, transitioning some of these spaces to allow for fluctuations in air capacity and storage via soft tissue borders. Other tetrapods independently underwent land-to-sea transitions, but it is unclear if they similarly changed their sinuses. We use computed tomography to study sinus changes in thalattosuchian crocodylomorphs that transformed from land-bound ancestors to become the only known aquatic swimming archosaurs. We find that thalattosuchian braincase sinuses reduced over their transition, similar to cetaceans, but their snout sinuses counterintuitively expanded, distinct from cetaceans, and that both trends were underpinned by high evolutionary rates. We hypothesize that aquatic thalattosuchians were ill suited to deep diving by their snout sinuses, which seem to have remained large to help drain their unusual salt glands. Thus, although convergent in general terms, thalattosuchians and cetaceans were subject to different constraints that shaped their transitions to water. Thalattosuchians attained a stage similar to less pelagic transitional forms in the cetacean lineage (late protocetid-basilosaurid) but did not become further specialized for ocean life.

The evolution of gestation length in eutherian mammals.

Eutherian mammals exhibit considerable variation in their gestation lengths, which has traditionally been linked to variation in other traits, including body mass and lifespan. To understand how gestation length variation, including its association with body mass and lifespan variation, changed over mammalian evolution, we conducted phylogeny-informed analyses of 845 representative extant species. We found that gestation length substantially differed in both whether and how strongly it was associated with body mass and lifespan across mammals. For example, gestation length was not associated with lifespan or body mass in Chiroptera and Cetacea but was strongly associated only with body mass in Carnivora. We also identified 52 evolutionary shifts in gestation length variation across the mammal phylogeny and 14 shifts when we jointly considered variation of all three traits; six shifts were shared. Notably, two of these shifts, both positive, occurred at the roots of Cetacea and Pinnipedia, respectively, coinciding with the transition of these clades to the marine environment, whereas a negative shift occurred at the root of Chiroptera, coinciding with the evolution of flight in this clade. These results suggest that the relationship between gestation length and the two other traits has varied substantially across mammalian phylogeny.

Social mating systems in birds: Resource-defense polygamy-but not lekking-is a macroevolutionarily unstable trait.

Our understanding of the evolution of social mating systems is largely based on an atemporal ecological framework, whereas macroevolutionary and phylogenetic perspectives looking at the causes of mating systems variation are less developed. Here, we present analyses of the evolution of social mating systems in birds at an unprecedented scale, including 66% of the world's birds and using trait-dependent speciation and extinction models. We found that lekking (no social bond between the sexes) is very rarely lost, in accordance with the hypothesis that a male shifting to investing in one rather than multiple mates would suffer a severe fitness cost. In contrast, resource-defense polygamous lineages (with a weak, transient socio-sexual bond) frequently revert back to monogamy (strong, durable socio-sexual bond) and have an elevated extinction fraction. We tentatively attribute this to the impossibility for females to settle on an optimal parental care strategy under this system. Finally, we found that most gains of lekking have been directly from monogamy, rather than through an intermediate stage of resource-defense polygamy.

Freshwater Habitats Promote Rapid Rates of Phenotypic Evolution in Sculpin Fishes (Perciformes: Cottoidea).

AbstractInvasions of freshwater habitats by marine fishes provide exceptional cases of habitat-driven biological diversification. Freshwater habitats make up less than 1% of aquatic habitats but contain ∼50% of fish species. However, while the dominant group of freshwater fishes (Otophysi) is older than that of most marine fishes (Percomorphaceae), it is less morphologically diverse. Classically, scientists have invoked differences in the tempo and/or mode of evolution to explain such cases of unequal morphological diversification. We tested for evidence of these phenomena in the superfamily Cottoidea (sculpins), which contains substantial radiations of marine and freshwater fishes. We find that the morphology of freshwater sculpins evolves faster but under higher constraint than that of marine sculpins, causing widespread convergence in freshwater sculpins and more morphological disparity in marine sculpins. The endemic freshwater sculpins of Lake Baikal, Siberia, are exceptions that demonstrate elevated novelty akin to that of marine sculpins. Several tantalizing factors may explain these findings, such as differences in habitat stability and/or habitat connectivity between marine and freshwater systems.

How life became colourful: colour vision, aposematism, sexual selection, flowers, and fruits.

Plants and animals are often adorned with potentially conspicuous colours (e.g. red, yellow, orange, blue, purple). These include the dazzling colours of fruits and flowers, the brilliant warning colours of frogs, snakes, and invertebrates, and the spectacular sexually selected colours of insects, fish, birds, and lizards. Such signals are often thought to utilize pre-existing sensitivities in the receiver's visual systems. This raises the question: what was the initial function of conspicuous colouration and colour vision? Here, we review the origins of colour vision, fruit, flowers, and aposematic and sexually selected colouration. We find that aposematic colouration is widely distributed across animals but relatively young, evolving only in the last ~150 million years (Myr). Sexually selected colouration in animals appears confined to arthropods and chordates, and is also relatively young (generally <100 Myr). Colourful flowers likely evolved ~200 million years ago (Mya), whereas colourful fruits/seeds likely evolved ~300 Mya. Colour vision (sensu lato) appears to be substantially older, and likely originated ~400-500 Mya in both arthropods and chordates. Thus, colour vision may have evolved long before extant lineages with fruit, flowers, aposematism, and sexual colour signals. We also find that there appears to have been an explosion of colour within the last ~100 Myr, including >200 origins of aposematic colouration across nine animal phyla and >100 origins of sexually selected colouration among arthropods and chordates.

Femora nutrient foramina and aerobic capacity in giant extinct xenarthrans.

Nutrient foramina are small openings in the periosteal surface of the mid-shaft region of long bones that traverse the cortical layer and reach the medullary cavity. They are important for the delivery of nutrients and oxygen to bone tissue and are crucial for the repair and remodeling of bones over time. The nutrient foramina in the femur's diaphysis are related to the energetic needs of the femur and have been shown to be related to the maximum metabolic rate (MMR) of taxa. Here, we investigate the relationship between nutrient foramen size and body mass as a proxy to the aerobic capacity of taxa in living and extinct xenarthrans, including living sloths, anteaters, and armadillos, as well as extinct xenarthrans such as glyptodonts, pampatheres, and ground sloths. Seventy femora were sampled, including 20 from extant taxa and 50 from extinct taxa. We obtained the blood flow rate (Q̇) based on foramina area and performed PGLS and phylogenetic ANCOVA in order to explore differences among mammalian groups. Our results show that, among mammals, taxa commonly associated with lower metabolism like living xenarthrans showed relatively smaller foramina, while the foramina of giant extinct xenarthrans like ground sloths and glyptodonts overlapped with non-xenarthran placentals. Consequently, Q̇ estimations indicated aerobic capacities comparable to other placental giant taxa like elephants or some ungulates. Furthermore, the estimation of the MMR for fossil giant taxa showed similar results, with almost all taxa showing high values except for those for which strong semi-arboreal or fossorial habits have been proposed. Moreover, the results are compatible with the diets predicted for extinct taxa, which indicate a strong consumption of grass similar to ungulates and in contrast to the folivorous or insectivorous diets of extant xenarthrans. The ancestral reconstruction of the MMR values indicated a lack of a common pattern for all xenarthrans, strongly supporting the occurrence of low metabolic rates in extant forms due to their particular dietary preferences and arboreal or fossorial habits. Our results highlight the importance of considering different evidence beyond the phylogenetic position of extinct taxa, especially when extinct forms are exceptionally different from their extant relatives. Future studies evaluating the energetic needs of giant extinct xenarthrans should not assume lower metabolic rates for these extinct animals based solely on their phylogenetic position and the observations on their extant relatives.

The Paradox of Predictability Provides a Bridge Between Micro- and Macroevolution.

The relationship between the evolutionary dynamics observed in contemporary populations (microevolution) and evolution on timescales of millions of years (macroevolution) has been a topic of considerable debate. Historically, this debate centers on inconsistencies between microevolutionary processes and macroevolutionary patterns. Here, we characterize a striking exception: emerging evidence indicates that standing variation in contemporary populations and macroevolutionary rates of phenotypic divergence are often positively correlated. This apparent consistency between micro- and macroevolution is paradoxical because it contradicts our previous understanding of phenotypic evolution and is so far unexplained. Here, we explore the prospects for bridging evolutionary timescales through an examination of this "paradox of predictability." We begin by explaining why the divergence-variance correlation is a paradox, followed by data analysis to show that the correlation is a general phenomenon across a broad range of temporal scales, from a few generations to tens of millions of years. Then we review complementary approaches from quantitative-genetics, comparative morphology, evo-devo, and paleontology to argue that they can help to address the paradox from the shared vantage point of recent work on evolvability. In conclusion, we recommend a methodological orientation that combines different kinds of short-term and long-term data using multiple analytical frameworks in an interdisciplinary research program. Such a program will increase our general understanding about how evolution works within and across timescales.

A macroevolutionary analysis of European Late Upper Palaeolithic stone tool shape using a Bayesian phylodynamic framework.

Phylogenetic models are commonly used in palaeobiology to study the patterns and processes of organismal evolution. In the human sciences, phylogenetic methods have been deployed for reconstructing ancestor-descendant relationships using linguistic and material culture data. Within evolutionary archaeology specifically, phylogenetic analyses based on maximum parsimony and discrete traits dominate, which sets limitations for the downstream role cultural phylogenies, once derived, can play in more elaborate analytical pipelines. Recent methodological advances in Bayesian phylogenetics, however, now allow us to infer evolutionary dynamics using continuous characters. Capitalizing on these developments, we here present an exploratory analysis of cultural macroevolution of projectile point shape evolution in the European Final Palaeolithic and earliest Mesolithic (approx. 15 000-11 000 BP) using a Bayesian phylodynamic approach and the fossilized birth-death process model. This model-based approach leaps far beyond the application of parsimony, in that it not only produces a tree, but also divergence times, and diversification rates while incorporating uncertainties. This allows us to compare rates to the pronounced climatic changes that occurred during our time frame. While common in cultural evolutionary analyses of language, the extension of Bayesian phylodynamic models to archaeology arguably represents a major methodological breakthrough.

The rise of dietary diversity in coral reef fishes.

Diet has been identified as a major driver of reef fish lineage diversification, producing one of the most speciose vertebrate assemblages today. Yet, there is minimal understanding of how, when and why diet itself has evolved. To address this, we used a comprehensive gut content dataset, alongside a recently developed phylogenetic comparative method to assess multivariate prey use across a diverse animal assemblage, coral reef fishes. Specifically, we investigated the diversification, transitions and phylogenetic conservatism of fish diets through evolutionary time. We found two major pulses of diet diversification: one at the end-Cretaceous and one during the Eocene, suggesting that the Cretaceous-Palaeogene mass extinction probably provided the initial ecological landscape for fish diets to diversify. The birth of modern families during the Eocene then provided the foundation for a second wave of dietary expansion. Together, our findings showcase the role of extinction rebound events in shaping the dietary diversity of fishes on present-day coral reefs.

Convergent expansions of keystone gene families drive metabolic innovation in a major eukaryotic clade.

Many remarkable innovations have repeatedly occurred across vast evolutionary distances. When convergent traits emerge on the tree of life, they are sometimes driven by the same underlying gene families, while other times many different gene families are involved. Conversely, a gene family may be repeatedly recruited for a single trait or many different traits. To understand the general rules governing convergence at both genomic and phenotypic levels, we systematically tested associations between 56 binary metabolic traits and gene count in 14,710 gene families from 993 species of Saccharomycotina yeasts. Using a recently developed phylogenetic approach that reduces spurious correlations, we discovered that gene family expansion and contraction was significantly linked to trait gain and loss in 45/56 (80%) of traits. While 601/746 (81%) of significant gene families were associated with only one trait, we also identified several 'keystone' gene families that were significantly associated with up to 13/56 (23%) of all traits. These results indicate that metabolic innovations in yeasts are governed by a narrow set of major genetic elements and mechanisms.

An evolutionary disruption of the buzz pollination syndrome in neotropical montane plants.

PREMISE: Under pollinator limitations, specialized pollination syndromes may evolve toward contrasting responses: a generalized syndrome with increased pollinator attraction, pollinator reward, and pollen transfer capacity; or the selfing syndrome with increased self-pollen deposition, but reduced pollinator attraction and pollen transfer capacity. The buzz-pollination syndrome is specialized to explore female vibrating bees as pollinators. However, vibrating bees become less-active pollinators at montane areas of the Atlantic Forest (AF) domain. This study investigated whether the specialized buzz-pollination syndrome would evolve toward an alternative floral syndrome in montane areas of the AF domain, considering a generalized and the selfing syndromes as alternative responses. METHODS: We utilized a lineage within the buzz-pollinated Miconia as study system, contrasting floral traits between montane AF-endemic and non-endemic species. We measured and validated floral traits that were proxies for pollinator attraction, reward access, pollen transfer capacity, and self-pollen deposition. We inferred the evolution of floral trait via phylogenetic comparative methods. RESULTS: AF-endemic species have selectively evolved greater reward access and more frequently had generalist pollination. Nonetheless, AF-endemic species also have selectively evolved toward lower pollen transfer capacity and greater self pollination. These patterns indicated a complex evolutionary process that has jointly favored a generalized and the selfing syndromes. CONCLUSIONS: The buzz pollination syndrome can undergo an evolutionary disruption in montane areas of the AF domain. This floral syndrome is likely more labile than often assumed, allowing buzz-pollinated plants to reproduce in environments where vibrating bees are less-reliable pollinators.

Gliding toward an understanding of the origin of flight in bats.

Bats are the only mammals capable of powered flight and have correspondingly specialized body plans, particularly in their limb morphology. The origin of bat flight is still not fully understood due to an uninformative fossil record but, from the perspective of a functional transition, it is widely hypothesized that bats evolved from gliding ancestors. Here, we test predictions of the gliding-to-flying hypothesis of the origin of bat flight by using phylogenetic comparative methods to model the evolution of forelimb and hindlimb traits on a dataset spanning four extinct bats and 231 extant mammals with diverse locomotor modes. Our results reveal that gliders exhibit adaptive trait optima (1) toward relatively elongate forelimbs that are intermediate between those of bats and non-gliding arborealists, and (2) toward relatively narrower but not longer hindlimbs that are intermediate between those of non-gliders and bats. We propose an adaptive landscape based on limb length and width optimal trends derived from our modeling analyses. Our results support a hypothetical evolutionary pathway wherein glider-like postcranial morphology precedes a bat-like morphology adapted to powered-flight, setting a foundation for future developmental, biomechanical, and evolutionary research to test this idea.

Commonly used Bayesian diversification methods lead to biologically meaningful differences in branch-specific rates on empirical phylogenies.

Identifying along which lineages shifts in diversification rates occur is a central goal of comparative phylogenetics; these shifts may coincide with key evolutionary events such as the development of novel morphological characters, the acquisition of adaptive traits, polyploidization or other structural genomic changes, or dispersal to a new habitat and subsequent increase in environmental niche space. However, while multiple methods now exist to estimate diversification rates and identify shifts using phylogenetic topologies, the appropriate use and accuracy of these methods are hotly debated. Here we test whether five Bayesian methods-Bayesian Analysis of Macroevolutionary Mixtures (BAMM), two implementations of the Lineage-Specific Birth-Death-Shift model (LSBDS and PESTO), the approximate Multi-Type Birth-Death model (MTBD; implemented in BEAST2), and the Cladogenetic Diversification Rate Shift model (ClaDS2)-produce comparable results. We apply each of these methods to a set of 65 empirical time-calibrated phylogenies and compare inferences of speciation rate, extinction rate, and net diversification rate. We find that the five methods often infer different speciation, extinction, and net-diversification rates. Consequently, these different estimates may lead to different interpretations of the macroevolutionary dynamics. The different estimates can be attributed to fundamental differences among the compared models. Therefore, the inference of shifts in diversification rates is strongly method dependent. We advise biologists to apply multiple methods to test the robustness of the conclusions or to carefully select the method based on the validity of the underlying model assumptions to their particular empirical system.

Decoupled evolution of ventral and dorsal scales in agamid lizards: ventral keels are associated with arboreality.

Arboreality has evolved in all major vertebrate lineages and is often associated with morphological adaptations and increased diversification concomitant with accessing novel niche space. In squamate reptiles, foot, claw, and tail morphology are well-studied adaptations shown to be associated with transitions to arboreality. Here, we examined a less well understood trait-the keeled scale-in relation to microhabitat, climate, and diversification dynamics across a diverse lizard radiation, Agamidae. We found that the ancestral agamid had keeled dorsal but not ventral scales; further, dorsal and ventral keels are evolutionarily decoupled. Ventral keeled scales evolved repeatedly in association with arboreality and may be advantageous in reducing wear or by promoting interlocking when climbing. We did not find an association between keeled scales and diversification, suggesting keels do not allow finer-scale microhabitat partitioning observed in other arboreal-associated traits. We additionally found a relationship between keeled ventral scales and precipitation in terrestrial species where we posit that the keels may function to reduce scale degradation. Our results suggest that keeled ventral scales facilitated transitions to arboreality across agamid lizards, and highlight a need for future studies that explore their biomechanical function in relation to microhabitat and climate.

Navigating uncertainty in maximum body size in marine metazoans.

Body size is a fundamental biological trait shaping ecological interactions, evolutionary processes, and our understanding of the structure and dynamics of marine communities on a global scale. Accurately defining a species' body size, despite the ease of measurement, poses significant challenges due to varied methodologies, tool usage, and subjectivity among researchers, resulting in multiple, often discrepant size estimates. These discrepancies, stemming from diverse measurement approaches and inherent variability, could substantially impact the reliability and precision of ecological and evolutionary studies reliant on body size data across extensive species datasets. This study examines the variation in reported maximum body sizes across 69,570 individual measurements of maximum size, ranging from <0.2 µm to >45 m, for 27,271 species of marine metazoans. The research aims to investigate how reported maximum size variations within species relate to organism size, taxonomy, habitat, and the presence of skeletal structures. The investigation particularly focuses on understanding why discrepancies in maximum size estimates arise and their potential implications for broader ecological and evolutionary studies relying on body size data. Variation in reported maximum sizes is zero for 38% of species, and low for most species, although it exceeds two orders of magnitude for some species. The likelihood of zero variation in maximum size decreased with more measurements and increased in larger species, though this varied across phyla and habitats. Pelagic organisms consistently had low maximum size range values, while small species with unspecified habitats had the highest variation. Variations in maximum size within a species were notably smaller than interspecific variation at higher taxonomic levels. Significant variation in maximum size estimates exists within marine species, and partially explained by organism size, taxonomic group, and habitat. Variation in maximum size could be reduced by standardized measurement protocols and improved meta-data. Despite the variation, egregious errors in published maximum size measurements are rare, and their impact on comparative macroecological and macroevolutionary research is likely minimal.

The seed morphospace, a new contribution towards the multidimensional study of angiosperm sexual reproductive biology.

BACKGROUND: The evolutionary success of flowering plants is associated with the vast diversity of their reproductive structures. Despite recent progress in understanding angiosperm-wide trends of floral structure and evolution, a synthetic view of the diversity in seed form and function across angiosperms is lacking. SCOPE: Here we present a roadmap to synthesise the diversity of seed forms in extant angiosperms, relying on the morphospace concept, i.e. a mathematical representation which relates multiple traits and describes the realised morphologies. We provide recommendations on how to broaden the range of measurable traits beyond mass, by using key morphological traits representative of the embryo, endosperm, and seed coat but also fruit attributes (e.g., dehiscence, fleshiness). These key traits were used to construct and analyse a morphospace to detect evolutionary trends and gain insight into how morphological traits relate to seed functions. Finally, we outline challenges and future research directions, combining the morphospace with macroevolutionary comparative methods to underline the drivers that gave rise to the diversity of observed seed forms. CONCLUSIONS: We conclude that this multidimensional approach has the potential, although still untapped, to improve our understanding of covariation among reproductive traits, and further elucidate angiosperm reproductive biology as a whole.