Joshua Robert Puzey

Plants strike a delicate balance between growth and defense. The calculus of how to defend against herbivores, and maximize growth and reproduction, can differ between annuals and perennials. Annuals have a live fast, reproduce young strategy; while perennials may maximize fecundity over years. Milkweed, a herbaceous perennial, is a mix of these two strategies. On one hand, a single individual milkweed ramet is functionally a herbaceous annual and vulnerable to herbivory. On the other hand, below ground connections allow plants to share resources and persist for multiple years, perhaps lowering the cost of localized herbivory. Here, we study the impact herbivory on the leaf and soil microbiome on milkweed growth and flowering in a naturally occurring population. Specifically, using milkweed populations at three different sites in Virginia, following individual ramets throughout the growth and flowering season, we quantified the soil and leaf microbiome through metagenomic shotgun sequencing. After controlling for plant size and plant genotype, we asked how the microbiome composition was related to flowering time and growth. We find that the leaf microbiome is a strong predictor of plant growth rate, but not flowering. Conversely, we find that the soil microbiome and plant size predict flowering probability. We found no evidence that herbivory altered the leaf or soil microbiome composition. Together these results provide evidence that plant microbiomes also influence growth and fecundity in natural populations of milkweed. These results also provide evidence that the leaf microbiome in milkweed is robust and stable in the face of significant herbivory. This study expands our knowledge of the contribution of plant microbiomes to plant demography in a clonal perennial plant.

Hybridisation affects the spatial and temporal patterns of morphological and genetic variation, shaping species evolution. Asclepias speciosa and A. syriaca provide an excellent system for uncovering how these patterns are generated. The ranges of A. speciosa and A. syriaca overlap on the North American Great Plains, and multiple intermediates are observed in this contact zone, consistent with hybridisation. However, other processes, such as preservation of ancestral polymorphism or selective pressure imposed by environmental clines, could explain the presence of morphological intermediates. In this study, we characterised patterns of variation within and between A. speciosa and A. syriaca using morphological and genetic data to validate the hybrid origin of intermediates, evaluate the impact of hybridisation on the parental species and reconstruct the demographic history of hybridisation events. In addition, we explored species‐specific associations of genetic variation with climatic variables. We demonstrated that hybridisation best explains the occurrence of large numbers of morphologically intermediate individuals in the contact zone and documented bidirectional and asymmetric genetic introgression. We found a strong relationship between precipitation patterns and genetic variation in A. speciosa and A. syriaca, which suggests that the hybrid zone is maintained by differences in annual precipitation. We discovered that the timing of secondary contact is relatively recent, coinciding with rapid range shifts during the Pleistocene. Our findings provide new insights into the dynamics of hybridisation on the North American Great Plains, the setting for numerous contact zones between taxa affiliated with eastern and western biotas.

Hybridization affects the spatial and temporal patterns of morphological and genetic variation, shaping species evolution. Asclepias speciosa and A. syriaca provide an excellent system for uncovering how these patterns are generated. The ranges of A. speciosa and A. syriaca overlap on the North American Great Plains, and multiple intermediates are observed in this contact zone, consistent with hybridization. However, other processes, such as preservation of ancestral polymorphism or selective pressure imposed by environmental clines, could explain the presence of morphological intermediates. In this study, we characterized patterns of variation within and between A. speciosa and A. syriaca using morphological and genetic data to validate the hybrid origin of intermediates, evaluate the impact of hybridization on the parental species, and reconstruct the demographic history of hybridization events. In addition, we explored species-specific associations of genetic variation with climatic variables. We demonstrated that hybridization best explains the occurrence of large numbers of morphologically intermediate individuals in the contact zone and documented bidirectional and asymmetric genetic introgression. We found a strong relationship between precipitation patterns and genetic variation in A. speciosa and A. syriaca, which suggests that the hybrid zone is maintained by differences in annual precipitation. We discovered that the timing of secondary contact is relatively recent, coinciding with rapid range shifts during the Pleistocene. Our findings provide new insights into the dynamics of hybridization on the North American Great Plains, the setting for numerous contact zones between taxa affiliated with eastern and western biotas.

Hybridization affects the spatial and temporal patterns of morphological and genetic variation, shaping species evolution. Asclepias speciosa and A. syriaca provide an excellent system for uncovering how these patterns are generated. The ranges of A. speciosa and A. syriaca overlap on the North American Great Plains, and multiple intermediates are observed in this contact zone, consistent with hybridization. However, other processes, such as preservation of ancestral polymorphism or selective pressure imposed by environmental clines, could explain the presence of morphological intermediates. In this study, we characterized patterns of variation within and between A. speciosa and A. syriaca using morphological and genetic data to validate the hybrid origin of intermediates, evaluate the impact of hybridization on the parental species, and reconstruct the demographic history of hybridization events. We demonstrate that hybridization best explains the occurrence of large numbers of morphologically intermediate individuals in the contact zone and document bidirectional and asymmetric genetic introgression. We discover that the timing of secondary contact is relatively recent, coinciding with rapid range shifts during the Pleistocene. Our findings provide new insights into the dynamics of hybridization on the North American Great Plains, the setting for numerous contact zones between taxa affiliated with eastern and western biotas.

The origin of phenotypic novelty is a perennial question of genetics and evolution. To date, few studies of biological pattern formation specifically address multi-generational aspects of inheritance and phenotypic novelty. For quantitative traits influenced by many segregating alleles, offspring phenotypes are often intermediate to parental values. In other cases, offspring phenotypes can be transgressive to parental values. For example, in the model organism Mimulus (monkeyflower), the offspring of parents with solid-colored petals exhibit novel spotted petal phenotypes. These patterns are controlled by an activator-inhibitor gene regulatory network with a small number of loci. Here we develop and analyze a model of hybridization and pattern formation that accounts for the inheritance of a diploid gene regulatory network composed of either homozygous or heterozygous alleles. We find that the resulting model of multi-generational Turing-type pattern formation can reproduce transgressive petal phenotypes similar to those observed in Mimulus. The model gives insight into how non-patterned parent phenotypes can yield phenotypically transgressive, patterned offspring, aiding in the development of empirically testable hypotheses.

The origin of phenotypic novelty is a perennial question of genetics and evolution. To date, few studies of biological pattern formation specifically address multi-generational aspects of inheritance and phenotypic novelty. For quantitative traits influenced by many segregating alleles, offspring phenotypes are often intermediate to parental values. In other cases, offspring phenotypes can be transgressive to parental values. For example, in the model organism Mimulus (monkeyflower), the offspring of parents with solid-colored petals exhibit novel spotted petal phenotypes. These patterns are controlled by an activator-inhibitor gene regulatory network with a small number of loci. Here we develop and analyze a model of hybridization and pattern formation that accounts for inheritance in diploid gene regulatory networks composed of either homozygous or heterozygous alleles. We find that the resulting model of multi-generational Turing-type pattern formation can reproduce the transgressive petal phenotypes observed in Mimulus . The model gives insight into how non-patterned parent phenotypes can yield phenotypically transgressive, patterned offspring, aiding in the development of empirically testable hypotheses.

The Plant Cell, Volume 33, Issue 7, koab117, https://doi.org/10.1093/plcell/koab117

Endosperm is an angiosperm innovation central to their reproduction whose development, and thus seed viability, is controlled by genomic imprinting, where expression from certain genes is parent-specific. Unsuccessful imprinting has been linked to failed inter-specific and inter-ploidy hybridization. Despite their importance in plant speciation, the underlying mechanisms behind these endosperm-based barriers remain poorly understood. Here, we describe one such barrier between diploid Mimulus guttatus and tetraploid Mimulus luteus. The two parents differ in endosperm DNA methylation, expression dynamics, and imprinted genes. Hybrid seeds suffer from underdeveloped endosperm, reducing viability, or arrested endosperm and seed abortion when M. guttatus or M. luteus is seed parent, respectively, and transgressive methylation and expression patterns emerge. The two inherited M. luteus subgenomes, genetically distinct but epigenetically similar, are expressionally dominant over the M. guttatus genome in hybrid embryos and especially their endosperm, where paternal imprints are perturbed. In aborted seeds, de novo methylation is inhibited, potentially owing to incompatible paternal instructions of imbalanced dosage from M. guttatus imprints. We suggest that diverged epigenetic/regulatory landscapes between parental genomes induce epigenetic repatterning and global shifts in expression, which, in endosperm, may uniquely facilitate incompatible interactions between divergent imprinting schemes, potentially driving rapid barriers.

In an empirical analysis of transposable element (TE) abundance within natural populations of Mimulus guttatus and Drosophila melanogaster , we found a surprisingly high variance of TE count (e.g., variance-to-mean ratio on the order of 10 to 300). To obtain insight regarding those evolutionary genetic mechanisms that are may underlie the overdispersed population distributions of TE abundance, we developed a mathematical model of TE population genetics that includes the dynamics of element proliferation and purifying selection on TE load. The modeling approach begins with a master equation for a birth-death process and extends the predictions of the classical theory of TE dynamics in several ways. In particular, moment-based analyses of time-dependent and equilibrium population distributions of TE load reveal that overdispersion is likely to arise via copy-and-paste proliferation dynamics, especially when the elementary processes of proliferation and excision are first-order and approximately balanced. Parameter studies and analytic work confirm this result and further suggest that overdispersed population distributions of TE abundance are unlikely to be a consequence of purifying selection on total element load.