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1. The geno-geo-climate nexus: contributions of geographic and ecological factors in shaping the genomic divergence of two closely related threatened rainforest species of Fontainea Heckel (Euphorbiaceae)

   https://doi.org/10.1007/s10980-024-01828-w  

   Brunton, Aaron J. ; Farleigh, Keaka ; Ogbourne, Steven M. ; Rossetto, Maurizio ; Schoeman, David S. ; Conroy, Gabriel C. ( January 2024 , Landscape Ecology)

   Processes that shape genomic and ecological divergence can reveal important evolutionary dynamics to inform the conservation of threatened species.Fontaineais a genus of rainforest shrubs and small trees including critically endangered and threatened species restricted to narrow, but complex geographic and ecological regions. Several species ofFontaineaare subject to spatially explicit conditions and experience limited intra-specific gene flow, likely generating genetic differentiation and local adaptation.

   Here, we explored the genetic and ecological mechanisms underlying patterns of diversification in two, closely related threatenedFontaineaspecies. Our aim was to compare spatial patterns of genetic variation between the vulnerableFontainea australis(Southern Fontainea) and critically endangeredF. oraria(Coastal Fontainea), endemic to the heterogeneous subtropical region of central, eastern Australia, where large-scale clearing has severely reduced rainforest habitat to a fraction (< 1%) of its pre-European settlement extent.

   We used a set of 10,000 reduced-representation markers to infer genetic relationships and the drivers of spatial genetic variation across the two species. In addition, we employed a combination of univariate and multivariate genome-environment association analysis using a set of topo-climatic variables to explore potential patterns of local adaptation as a factor impacting genomic divergence.

   Our study revealed that Coastal Fontainea have a close genetic relationship with Southern Fontainea. We showed that isolation by distance has played a key role in their genetic variation, indicating that vicariance can explain the spatial genetic distribution of the two species. Genotype-environment analyses showed a strong association with temperature and topographic features, suggesting adaptation to localised thermal environments. We used a multivariate redundancy analysis to identify a range of putatively adapted loci associated with local environmental conditions.

   Divergent selection at the local-habitat scale as a result of dispersal limitations and environmental heterogeneity (including physical barriers) are likely contributors to adaptive divergence between the twoFontaineaspecies. Our findings have presented evidence to indicate that Southern and Coastal Fontainea were comprised of distinct genetic groups and ecotypes, that together may form a single species continuum, with further phenotype research suggested to confirm the current species boundaries. Proactive conservation actions, including assisted migration to enhance the resilience of populations lacking stress-tolerant single nucleotide polymorphisms (SNPs) may be required to secure the long-term future of both taxa. This is especially vital for the critically endangered Coastal Fontainea given projections of habitat decline for the species under future climate scenarios.

    

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2. Notes from the taxonomic disaster zone: Evolutionary drivers of intractable species boundaries in an Australian lizard clade (Scincidae: Ctenotus )

   https://doi.org/10.1111/mec.17074  

   Prates, Ivan ; Hutchinson, Mark N. ; Singhal, Sonal ; Moritz, Craig ; Rabosky, Daniel L. ( July 2023 , Molecular Ecology)

   Genomic‐scale datasets, sophisticated analytical techniques, and conceptual advances have disproportionately failed to resolve species boundaries in some groups relative to others. To understand the processes that underlie taxonomic intractability, we dissect the speciation history of an Australian lizard clade that arguably represents a “worst‐case” scenario for species delimitation within vertebrates: theCtenotus inornatusspecies group, a clade beset with decoupled genetic and phenotypic breaks, uncertain geographic ranges, and parallelism in purportedly diagnostic morphological characters. We sampled hundreds of localities to generate a genomic perspective on population divergence, structure, and admixture. Our results revealed rampant paraphyly of nominate taxa in the group, with lineages that are either morphologically cryptic or polytypic. Isolation‐by‐distance patterns reflect spatially continuous differentiation among certain pairs of putative species, yet genetic and geographic distances are decoupled in other pairs. Comparisons of mitochondrial and nuclear gene trees, tests of nuclear introgression, and historical demographic modelling identified gene flow between divergent candidate species. Levels of admixture are decoupled from phylogenetic relatedness; gene flow is often higher between sympatric species than between parapatric populations of the same species. Such idiosyncratic patterns of introgression contribute to species boundaries that are fuzzy while also varying in fuzziness. Our results suggest that “taxonomic disaster zones” like theC. inornatusspecies group result from spatial variation in the porosity of species boundaries and the resulting patterns of genetic and phenotypic variation. This study raises questions about the origin and persistence of hybridizing species and highlights the unique insights provided by taxa that have long eluded straightforward taxonomic categorization.

    

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3. Discerning structure versus speciation in phylogeographic analysis of Seepage Salamanders ( Desmognathus aeneus ) using demography, environment, geography, and phenotype

   https://doi.org/10.1111/mec.17219  

   Pyron, R. Alexander ; Kakkera, Anvith ; Beamer, David A. ; O'Connell, Kyle A. ( November 2023 , Molecular Ecology)

   Numerous mechanisms can drive speciation, including isolation by adaptation, distance, and environment. These forces can promote genetic and phenotypic differentiation of local populations, the formation of phylogeographic lineages, and ultimately, completed speciation. However, conceptually similar mechanisms may also result in stabilizing rather than diversifying selection, leading to lineage integration and the long‐term persistence of population structure within genetically cohesive species. Processes that drive the formation and maintenance of geographic genetic diversity while facilitating high rates of migration and limiting phenotypic differentiation may thereby result in population genetic structure that is not accompanied by reproductive isolation. We suggest that this framework can be applied more broadly to address the classic dilemma of “structure” versus “species” when evaluating phylogeographic diversity, unifying population genetics, species delimitation, and the underlying study of speciation. We demonstrate one such instance in the Seepage Salamander (Desmognathus aeneus) from the southeastern United States. Recent studies estimated up to 6.3% mitochondrial divergence and four phylogenomic lineages with broad admixture across geographic hybrid zones, which could potentially represent distinct species supported by our species‐delimitation analyses. However, while limited dispersal promotes substantial isolation by distance, microhabitat specificity appears to yield stabilizing selection on a single, uniform, ecologically mediated phenotype. As a result, climatic cycles promote recurrent contact between lineages and repeated instances of high migration through time. Subsequent hybridization is apparently not counteracted by adaptive differentiation limiting introgression, leaving a single unified species with deeply divergent phylogeographic lineages that nonetheless do not appear to represent incipient species.

    

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4. Phylogeography and population genetics reveal ring species patterns in a highly polymorphic California lily

   https://doi.org/10.1111/jbi.14313  

   Hernández, Adriana I. ; Landis, Jacob B. ; Specht, Chelsea D. ( January 2022 , Journal of Biogeography)

   Natural selection typically results in the homogenization of reproductive traits, reducing natural variation within populations; thus, highly polymorphic species present unresolved questions regarding the mechanisms that shape and maintain gene flow given a diversity of phenotypes. We used an integrative framework to characterize phenotypic diversity and assess how evolutionary history and population genetics affect the highly polymorphic nature of a California endemic lily.

   California, United States.

   Butterfly mariposa lily,Calochortus venustus(Liliaceae).

   We summarized phenotypic diversity at both metapopulation and subpopulation scales to explore spatial phenotypic distributions. We sampled 174 individuals across the species range representing multiple samples for each population and each phenotype. We used restriction‐site‐associated DNA sequencing (RAD‐Seq) to detect population clusters, gene flow between phenotypes and between populations, infer haplotype networks, and reconstruct ancestral range evolution to infer historical migration and range expansion.

   Polymorphic floral traits within the species such as petal pigmentation and distal spots are geographically structured, and inferred evolutionary history is consistent with a ring species pattern involving a complex of populations having experienced sequential change in genetic and phenotypic variation from the founding population. Populations remain interconnected yet have differentiated from each other along a bifurcating south‐to‐north range expansion, consequently indicating parallel evolution towards the white morphotype in the northern range. Thus, our phylogeographical analyses reveal morphological convergence with population genetic cohesion irrespective of phenotypic diversity.

   Phenotypic variation in the highly polymorphicCalochortus venustusis not due to genetic differentiation between phenotypes; rather there is genetic cohesion within six geographically defined populations, some of which maintain a high level of within‐population phenotypic diversity. Our results demonstrate that analyses of polymorphic taxa greatly benefit from disentangling phenotype from genotype at various spatial scales. We discuss results in light of ring species concepts and the need to determine the adaptive significance of the patterns we report.

    

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5. Experimental and genetic analysis of selfing reveals no reinforcement in Phlox cuspidata

   https://doi.org/10.1086/729299  

   Shahid, Bushra M. ; Burgin, Grace A. ; Hopkins, Robin ( January 2024 , International Journal of Plant Sciences)

   • Reinforcement is the process through which prezygotic reproductive barriers evolve in sympatry due to selection against hybridization between co-occurring, closely related species. The role of self-fertilization in reinforcement and reproductive isolation is uncertain in part because its efficiency as a barrier against heterospecific mating can depend on the timing of autonomous selfing. • To investigate whether increased autonomous selfing has evolved as a mechanism for reinforcement, we compared Phlox cuspidata populations across their native Texas range using both estimates of genetic diversity and experimental manipulation with morphological measurements. Specifically, we investigated patterns of variation in floral traits and timing of selfing between individuals from allopatric populations of P. cuspidata and from populations sympatric with the closely related species, P. drummondii. • We infer intermediate rates of selfing across field-collected individuals with no significant difference between allopatric and sympatric populations. Among greenhouse grown plants, we find no differences in timing of selfing or other floral traits including anther dehiscence timing, anther-stigma distances, autonomous selfing rate and self-seed count between allopatric and sympatric populations. However, our statistical analyses indicate that P. cuspidata individuals sympatric with P drummondii seem to have generally larger flowers compared to allopatric individuals. • Despite strong evidence of costly hybridization with P. drummondii, we find no evidence of trait divergence due to reinforcement in P. cuspidata. Although we document nearly complete autonomous self-seed set in the greenhouse, estimates of selfing rates from genetic data imply realized selfing is much lower in nature suggesting an opportunity for reinforcing selection to act on this trait. 

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