Three new Cenomanian conifers from El Chango (Chiapas, Mexico) offer a snapshot of the geographic mosaic of the Mesozoic conifer decline

Premise of study: El Chango is a recently discovered quarry that contains extremely well preserved fossils. The Cenomanian age of the locality corresponds to a time when the global flora was transitioning from gymnosperm- to angiosperm-dominated, yet conifers predominate in this locality. These fossils thus provide a rare opportunity to understand the replacement of conifers by angiosperms as the dominant group of plants. Methods: We collected material from El Chango in annual expeditions (2010 to 2014). We selected the three most abundant and best preserved conifer morphotypes and conducted a total-evidence (i.e., including molecular and morphological data) phylogenetic analysis of a sample of 72 extant conifer species plus the three fossils. We use these results to inform our taxonomic decisions. Results: We obtained four equally most-parsimonious trees (consistency index = 44.1%, retention index = 78.8%). Despite ambiguous relationships among some extant taxa, the three fossil conifers had the same phylogenetic position in all four most parsimonious trees; we describe these species as new: Sequoiadendron helicalancifolium sp. nov. (Cupressaceae), and Microcachrys rhomboidea sp. nov. and Dacrydium bifoliosus sp. nov (Podocarpaceae). The ecosystem is interpreted as a coastal humid mixed forest. Conclusions: Our findings contribute to the understanding of Cenomanian equatorialregions, and support the hypothesis of a geographically and ecologically structured rise of angiosperms, with conifers remaining dominant in brackish-water and angiosperms becoming dominant in freshwater-ecosystems. These fossils fill in gaps in the evolutionary history of lineages like Microcachrys, which we demonstrate occurred in the Northern hemisphere before becoming restricted to its current range (Tasmania).

Interacting Phenotypes and the Coevolutionary Process

Coevolution occurs when species interact to influence one another’s fitness, resulting in reciprocal evolutionary change. In many coevolving lineages, trait expression in one species is modified by the genotypes and phenotypes of the other, forming feedback loops reminiscent of models of intraspecific social evolution. Here, we adapt the theory of within-species social evolution, characterized by indirect genetic effects and social selection imposed by interacting individuals, to the case of interspecific interactions. In a trait-based model, we derive general expressions for multivariate evolutionary change in two species and the expected between-species covariance in evolutionary change across a selection mosaic. We show that reciprocal interspecific indirect genetic effects can dominate the coevolutionary process and drive patterns of correlated evolution beyond what is expected from direct selection alone. In extreme cases, interspecific indirect genetic effects can lead to coevolution when selection does not covary between species or even when one species lacks genetic variance. Moreover, our model indicates that interspecific indirect genetic effects may interact in complex ways with cross-species selection to determine the course of coevolution. Importantly, our model makes empirically testable predictions for how different forms of reciprocal interactions contribute to the coevolutionary process and influence the geographic mosaic of coevolution.

Geographic Mosaics of Fly Pollinators With Divergent Color Preferences Drive Landscape-Scale Structuring of Flower Color in Daisy Communities

The striking variation in flower color across and within Angiosperm species is often attributed to divergent selection resulting from geographic mosaics of pollinators with different color preferences. Despite the importance of pollinator mosaics in driving floral divergence, the distributions of pollinators and their color preferences are seldom quantified. The extensive mass-flowering displays of annual daisy species in Namaqualand, South Africa, are characterized by striking color convergence within communities, but also color turnover within species and genera across large geographic scales. We aimed to determine whether shifts between orange and white-flowered daisy communities are driven by the innate color preferences of different pollinators or by soil color, which can potentially affect the detectability of different colored flowers. Different bee-fly pollinators dominated in both community types so that largely non-overlapping pollinator distributions were strongly associated with different flower colors. Visual modeling demonstrated that orange and white-flowered species are distinguishable in fly vision, and choice experiments demonstrated strongly divergent color preferences. We found that the dominant pollinator in orange communities has a strong spontaneous preference for orange flowers, which was not altered by conditioning. Similarly, the dominant pollinator in white communities exhibited an innate preference for white flowers. Although detectability of white flowers varied across soil types, background contrast did not alter color preferences. These findings demonstrate that landscape-level flower color turnover across Namaqua daisy communities is likely shaped by a strong qualitative geographic mosaic of bee-fly pollinators with divergent color preferences. This is an unexpected result given the classically generalist pollination phenotype of daisies. However, because of the dominance of single fly pollinator species within communities, and the virtual absence of bees as pollinators, we suggest that Namaqua daisies function as pollination specialists despite their generalist phenotypes, thus facilitating differentiation of flower color by pollinator shifts across the fly pollinator mosaic.

Allopatric divergence limits cheating range and alters genetic requirements for a cooperative trait

Social and genomic context may constrain the fates of mutations in cooperation genes. While some mechanisms limiting cheaters evolve in the presence of cheating, here we ask whether cheater resistance can evolve latently even in environments where cooperation is not expressed and cheaters are absent. The bacterium Myxococcus xanthus undergoes cooperative multicellular development upon starvation, but developmentally defective cheaters can outcompete cooperators within mixed groups. Using natural isolates and an obligate cheater disrupted at the developmental-signaling gene csgA, we show that cheating range is narrow among natural strains due to antagonisms that do not specifically target cheaters. Further, we mixed the cheater with closely related cooperators that diverged from it allopatrically in nutrient-rich environments in which cooperative development does not occur, showing that even slight divergence under these conditions can eliminate cheating phenotypes. Our results suggest that such cooperation- and cheater-blind divergence can generate a geographic mosaic of local cheater-cooperator compatibility patches that limit cheater spread. We also ask whether genomic divergence can shape the fitness effects of disrupting a cooperation gene. Construction of the same csgA mutation in several natural-isolate cooperators generated a wide range of pure-culture sporulation phenotypes, from a complete defect to no defect. Thus, we find that epistatic interactions limit the range of genomes within which a mutation creates a cooperation defect. Moreover, these results reveal Developmental System Drift in a microbial system because sporulation proficiency is conserved across the natural isolates despite divergence in the role of csgA.

The scales of coevolution: comparative phylogeography and genetic demography of a locally adapted venomous predator and its prey

Coevolutionary theory predicts that differences in the genetic demography of interacting species can influence patterns of local adaptation by affecting the potential of local populations to respond to selection. We conducted a comparative phylogeographical study of venomous rattlesnakes and their venom-resistant ground squirrel prey across California, and assessed how effective population size (Ne) estimates correspond with a previously documented pattern of rattlesnake local adaptation. Using RAD sequencing markers, we detected lineage relationships among both the rattlesnakes (Crotalus oreganus ssp.) and ground squirrels (Otospermophilus sp.) that are incongruent with previous phylogenetic hypotheses. Both rattlesnakes and squirrels share a deep divergence at the Sacramento–San Joaquin River Delta. At this broad phylogeographical scale, we found that the locally adapted rattlesnakes had higher Ne than squirrels. At the population scale, snakes also had larger Ne accompanied by larger values of several metrics of population genetic diversity. However, the specific magnitude of local adaptation of venom activity to ground squirrel venom resistance was not significantly correlated with local differences in Ne or other diversity statistics between predator and prey populations, suggesting that other factors in the geographic mosaic of coevolution contribute to the specific local-scale outcomes of this interaction. These results suggest an evolutionary mechanism that may explain some (but clearly not all) of rattlesnake local adaptation in this coevolutionary interaction – larger population sizes raise the adaptive potential of rattlesnakes compared to ground squirrels.

Strong Gene Flow Undermines Local Adaptations in a Host Parasite System

The co-evolutionary pathways followed by hosts and parasites strongly depend on the adaptive potential of antagonists and its underlying genetic architecture. Geographically structured populations of interacting species often experience local differences in the strength of reciprocal selection pressures, which can result in a geographic mosaic of co-evolution. One example of such a system is the boreo-montane social wasp Polistes biglumis and its social parasite Polistes atrimandibularis, which have evolved local defense and counter-defense mechanisms to match their antagonist. In this work, we study spatial genetic structure of P. biglumis and P. atrimandibularis populations at local and regional scales in the Alps, by using nuclear markers (DNA microsatellites, AFLP) and mitochondrial sequences. Both the host and the parasite populations harbored similar amounts of genetic variation. Host populations were not genetically structured at the local scale, but geographic regions were significantly differentiated from each other in both the host and the parasite in all markers. The net dispersal inferred from genetic differentiation was similar in the host and the parasite, which may be due to the annual migration pattern of the parasites between alpine and lowland populations. Thus, the apparent dispersal barriers (i.e., high mountains) do not restrict gene flow as expected and there are no important gene flow differences between the species, which contradict the hypothesis that restricted gene flow is required for local adaptations to evolve.