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1. The paradox behind the pattern of rapid adaptive radiation: how can the speciation process sustain itself through an early burst?

   Martin, CH ; Richards, EJ ( January 2019 , Annual review of ecology, evolution, and systematics)

   Rapid adaptive radiation poses a distinct question apart from speciation and adaptation: what happens after one speciation event? That is, how are some lineages able to continue speciating through a rapid burst? This question connects global macroevolutionary patterns to microevolutionary processes. Here we review major features of rapid radiations in nature and their mismatch with theoretical models and what is currently known about speciation mechanisms. Rapid radiations occur on three major diversification axes – species richness, phenotypic disparity, and ecological diversity – with exceptional outliers on each axis. The paradox is that the hallmark early stage of adaptive radiation, a rapid burst of speciation and niche diversification, is contradicted by most existing speciation models which instead predict continuously decelerating speciation rates and niche subdivision through time. Furthermore, while speciation mechanisms such as magic traits, phenotype matching, and physical linkage of co-adapted alleles promote speciation, it is often not discussed how these mechanisms could promote multiple speciation events in rapid succession. Additional mechanisms beyond ecological opportunity are needed to understand how rapid radiations occur. We review the evidence for five emerging theories: 1) the ‘transporter’ hypothesis: introgression and the ancient origins of adaptive alleles, 2) the ‘signal complexity’ hypothesis: the dimensionality of sexual traits, 3) the connectivity of fitness landscapes, 4) ‘diversity begets diversity’, and 5) flexible stem/‘plasticity first’. We propose new questions and predictions to guide future work on the mechanisms underlying the rare origins of rapid radiation. 

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2. Resolving Marine–Freshwater Transitions by Diatoms Through a Fog of Gene Tree Discordance

   https://doi.org/10.1093/sysbio/syad038  

   Roberts, Wade R. ; Ruck, Elizabeth C. ; Downey, Kala M. ; Pinseel, Eveline ; Alverson, Andrew J. ; Smith, ed., Stacey ( June 2023 , Systematic Biology)

   Despite the obstacles facing marine colonists, most lineages of aquatic organisms have colonized and diversified in freshwaters repeatedly. These transitions can trigger rapid morphological or physiological change and, on longer timescales, lead to increased rates of speciation and extinction. Diatoms are a lineage of ancestrally marine microalgae that have diversified throughout freshwater habitats worldwide. We generated a phylogenomic data set of genomes and transcriptomes for 59 diatom taxa to resolve freshwater transitions in one lineage, the Thalassiosirales. Although most parts of the species tree were consistently resolved with strong support, we had difficulties resolving a Paleocene radiation, which affected the placement of one freshwater lineage. This and other parts of the tree were characterized by high levels of gene tree discordance caused by incomplete lineage sorting and low phylogenetic signal. Despite differences in species trees inferred from concatenation versus summary methods and codons versus amino acids, traditional methods of ancestral state reconstruction supported six transitions into freshwaters, two of which led to subsequent species diversification. Evidence from gene trees, protein alignments, and diatom life history together suggest that habitat transitions were largely the product of homoplasy rather than hemiplasy, a condition where transitions occur on branches in gene trees not shared with the species tree. Nevertheless, we identified a set of putatively hemiplasious genes, many of which have been associated with shifts to low salinity, indicating that hemiplasy played a small but potentially important role in freshwater adaptation. Accounting for differences in evolutionary outcomes, in which some taxa became locked into freshwaters while others were able to return to the ocean or become salinity generalists, might help further distinguish different sources of adaptive mutation in freshwater diatoms.

    

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3. Divergent diapause life history timing drives both allochronic speciation and reticulate hybridization in an adaptive radiation of Rhagoletis flies

   https://doi.org/10.1111/mec.15908  

   Inskeep, Katherine A. ; Doellman, Meredith M. ; Powell, Thomas H. Q. ; Berlocher, Stewart H. ; Seifert, Nicholas R. ; Hood, Glen R. ; Ragland, Gregory J. ; Meyers, Peter J. ; Feder, Jeffrey L. ( April 2021 , Molecular Ecology)

   Divergent adaptation to new ecological opportunities can be an important factor initiating speciation. However, as niches are filled during adaptive radiations, trait divergence driving reproductive isolation between sister taxa may also result in trait convergence with more distantly related taxa, increasing the potential for reticulated gene flow across the radiation. Here, we demonstrate such a scenario in a recent adaptive radiation ofRhagoletisfruit flies, specialized on different host plants. Throughout this radiation, shifts to novel hosts are associated with changes in diapause life history timing, which act as “magic traits” generating allochronic reproductive isolation and facilitating speciation‐with‐gene‐flow. Evidence from laboratory rearing experiments measuring adult emergence timing and genome‐wide DNA‐sequencing surveys supported allochronic speciation between summer‐fruitingVacciniumspp.‐infestingRhagoletis mendaxand its hypothesized and undescribed sister taxon infesting autumn‐fruiting sparkleberries. The sparkleberry fly andR. mendaxwere shown to be genetically discrete sister taxa, exhibiting no detectable gene flow and allochronically isolated by a 2‐month average difference in emergence time corresponding to host availability. At sympatric sites across the southern USA, the later fruiting phenology of sparkleberries overlaps with that of flowering dogwood, the host of another more distantly related and undescribedRhagoletistaxon. Laboratory emergence data confirmed broadly overlapping life history timing and genomic evidence supported on‐going gene flow between sparkleberry and flowering dogwood flies. Thus, divergent phenological adaptation can drive the initiation of reproductive isolation, while also enhancing genetic exchange across broader adaptive radiations, potentially serving as a source of novel genotypic variation and accentuating further diversification.

    

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4. Niche expansion and adaptive divergence in the global radiation of crows and ravens

   https://doi.org/10.1038/s41467-022-29707-5  

   Garcia-Porta, Joan ; Sol, Daniel ; Pennell, Matt ; Sayol, Ferran ; Kaliontzopoulou, Antigoni ; Botero, Carlos A. ( April 2022 , Nature Communications)

   The processes that allow some lineages to diversify rapidly at a global scale remain poorly understood. Although earlier studies emphasized the importance of dispersal, global expansions expose populations to novel environments and may also require adaptation and diversification across new niches. In this study, we investigated the contributions of these processes to the global radiation of crows and ravens (genusCorvus). Combining a new phylogeny with comprehensive phenotypic and climatic data, we show thatCorvusexperienced a massive expansion of the climatic niche that was coupled with a substantial increase in the rates of species and phenotypic diversification. The initiation of these processes coincided with the evolution of traits that promoted dispersal and niche expansion. Our findings suggest that rapid global radiations may be better understood as processes in which high dispersal abilities synergise with traits that, like cognition, facilitate persistence in new environments.

    

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5. Diversification along a benthic to pelagic gradient contributes to fish diversity in the world's largest lake (Lake Baikal, Russia)

   https://doi.org/10.1111/mec.16209  

   St. John, Carl A. ; Buser, Thaddaeus J. ; Kee, Victoria E. ; Kirilchik, Sergei ; Bogdanov, Bakhtiar ; Neely, David ; Sandel, Michael ; Aguilar, Andres ( October 2021 , Molecular Ecology)

   Insights into the generation of diversity in both plants and animals have relied heavily on studying speciation in adaptive radiations. Russia's Lake Baikal has facilitated a putative adaptive radiation of cottid fishes (sculpins), some of which are highly specialized to inhabit novel niches created by the lake's unique geology and ecology. Here, we test evolutionary relationships and novel morphological adaptation in a piece of this radiation: the Baikal cottid genus,Cottocomephorus, a morphologically derived benthopelagic genus of three described species. We used a combination of mitochondrial DNA and restriction site associated DNA sequencing from allCottocomephorusspecies. Analysis of mitochondrial cytochrome b haplotypes was only able to two resolve two lineages:C. grewingkiiandC. comephoroides/inermis. Phylogenetic inference, principal component analysis, andfaststructureof genome‐wide SNPs uncovered three lineages withinCottocomephorus:C. comephoroides,C. inermisandC. grewingkii. We found recent divergence and admixture betweenC. comephoroidesandC. inermisand deep divergence between these two species andC. grewingkii. Contrasting other fish radiations, we found no evidence of ancient hybridization amongCottocomephorusspecies. Digital morphology revealed highly derived pelagic phenotypes that reflect divergence by specialization to the benthopelagic niche inCottocomephorus. AmongCottocomephorusspecies, we found evidence of ongoing adaptation to the pelagic zone. This pattern highlights the importance of speciation along a benthic‐pelagic gradient seen inCottocomephorusand across other adaptive fish radiations.

    

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