Developmental constraint shaped genome evolution and erythrocyte loss in Antarctic fishes following paleoclimate change

In the frigid, oxygen-rich Southern Ocean (SO), Antarctic icefishes (Channichthyidae; Notothenioidei) evolved the ability to survive without producing erythrocytes and hemoglobin, the oxygen-transport system of virtually all vertebrates. Here, we integrate paleoclimate records with an extensive phylogenomic dataset of notothenioid fishes to understand the evolution of trait loss associated with climate change. In contrast to buoyancy adaptations in this clade, we find relaxed selection on the genetic regions controlling erythropoiesis evolved only after sustained cooling in the SO. This pattern is seen not only within icefishes but also occurred independently in other high-latitude notothenioids. We show that one species of the red-blooded dragonfish clade evolved a spherocytic anemia that phenocopies human patients with this disease via orthologous mutations. The genomic imprint of SO climate change is biased toward erythrocyte-associated conserved noncoding elements (CNEs) rather than to coding regions, which are largely preserved through pleiotropy. The drift in CNEs is specifically enriched near genes that are preferentially expressed late in erythropoiesis. Furthermore, we find that the hematopoietic marrow of icefish species retained proerythroblasts, which indicates that early erythroid development remains intact. Our results provide a framework for understanding the interactions between development and the genome in shaping the response of species to climate change.

Are our phylomorphospace plots so terribly tangled? An investigation of disorder in data simulated under adaptive and nonadaptive models

Contemporary methods for visualizing phenotypic evolution, such as phylomorphospaces, often reveal patterns which depart strongly from a naïve expectation of consistently divergent branching and expansion. Instead, branches regularly crisscross as convergence, reversals, or other forms of homoplasy occur, forming patterns described as “birds’ nests”, “flies in vials”, or less elegantly, “a mess”. In other words, the phenotypic tree of life often appears highly tangled. Various explanations are given for this, such as differential degrees of developmental constraint, adaptation, or lack of adaptation. However, null expectations for the magnitude of disorder or “tangling” have never been established, so it is unclear which or even whether various evolutionary factors are required to explain messy patterns of evolution. I simulated evolution along phylogenies under a number of varying parameters (number of taxa and number of traits) and models (Brownian motion, Ornstein–Uhlenbeck (OU)-based, early burst, and character displacement (CD)] and quantified disorder using 2 measures. All models produce substantial amounts of disorder. Disorder increases with tree size and the number of phenotypic traits. OU models produced the largest amounts of disorder—adaptive peaks influence lineages to evolve within restricted areas, with concomitant increases in crossing of branches and density of evolution. Large early changes in trait values can be important in minimizing disorder. CD consistently produced trees with low (but not absent) disorder. Overall, neither constraints nor a lack of adaptation is required to explain messy phylomorphospaces—both stochastic and deterministic processes can act to produce the tantalizingly tangled phenotypic tree of life.

A mechanical cusp catastrophe imposes a universal developmental constraint on the shapes of tip-growing cells

Understanding the mechanistic basis for cell morphology is a central problem in biology. Evolution has converged on tip growth many times, yielding filamentous cells, yet tip-growing cells display a range of apical morphologies. To understand this variability, we measured the spatial profiles of cell-wall expansion for three species that spanned the phylogeny and morphology of tip-growth. Profiles were consistent with a mechanical model whereby the wall was stratified and stretched by turgor pressure during cell growth. We calculated the spatial profiles of wall mechanical properties, which could be accurately fit with an empirical two-parameter function. Combined with the mechanical model, this function yielded a “morphospace” that accounted for the shapes of diverse tip-growing species. However, natural shapes were bounded by a cusp bifurcation in the morphospace that separated thin, fast-growing cells from (nonexistent) wide, slow-growing cells. This constraint has important implications for our understanding of the evolution of tip-growing cells.

Modularity increases rate of floral evolution and adaptive success for functionally specialized pollination systems

Angiosperm flowers have diversified in adaptation to pollinators, but are also shaped by developmental and genetic histories. The relative importance of these factors in structuring floral diversity remains unknown. We assess the effects of development, function and evolutionary history by testing competing hypotheses on floral modularity and shape evolution in Merianieae (Melastomataceae). Merianieae are characterized by different pollinator selection regimes and a developmental constraint: tubular anthers adapted to specialized buzz-pollination. Our analyses of tomography-based 3-dimensional flower models show that pollinators selected for functional modules across developmental units and that patterns of floral modularity changed during pollinator shifts. Further, we show that modularity was crucial for Merianieae to overcome the constraint of their tubular anthers through increased rates of evolution in other flower parts. We conclude that modularity may be key to the adaptive success of functionally specialized pollination systems by making flowers flexible (evolvable) for adaptation to changing selection regimes.

Convergent evolution of sex-specific leg ornaments in Drosophilidae – from cells to structures

Sexually dimorphic morphological traits are among the fastest evolving animal features. Similar sex-specific structures have sometimes evolved independently in multiple lineages, presumably as targets of parallel sexual selection. In such cases, comparing the cellular mechanisms that generate these structures in different species can elucidate the interplay between selection and developmental constraint in evolution. In Drosophilidae, male-specific tarsal brushes on the front legs are found in at least four separate lineages. In this study, we combine phylogenetic reconstruction with developmental analyses and behavioral observations to investigate the evolutionary origin of these structures. We show that the sex brush has evolved independently at least three times from sexually monomorphic ancestral morphology. However, all sex brushes have very similar fine structure and develop through indistinguishable cellular processes, providing a striking example of developmental convergence. In all examined species, males use their sex brushes to grasp the female abdomen prior to copulation. We discuss potential reasons why convergent evolution of novel structures is rare even in the face of similar functional demands.