Rapid adaptive radiation poses two distinct questions apart from speciation and adaptation: What happens after one speciation event and how do some lineages continue speciating through a rapid burst? We review major features of rapid radiations and their mismatch with theoretical models and speciation mechanisms. The paradox is that the hallmark rapid burst pattern of adaptive radiation is contradicted by most speciation models, which predict continuously decelerating diversification and niche subdivision. Furthermore, it is unclear if and how speciation-promoting mechanisms such as magic traits, phenotype matching, and physical linkage of coadapted alleles promote rapid bursts of speciation. We review additional mechanisms beyond ecological opportunity to explain rapid radiations: ( a) ancient adaptive alleles and the transporter hypothesis, ( b) sexual signal complexity, ( c) fitness landscape connectivity, ( d) diversity begets diversity, and ( e) plasticity first. We propose new questions and predictions connecting microevolutionary processes to macroevolutionary patterns through the study of rapid radiations.
To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of adaptive alleles underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. On a single Bahamian island, ancient standing variation from disjunct geographic sources was reassembled into new combinations under strong directional selection for adaptation to the novel trophic niches of scale-eating and molluscivory. We found evidence for two longstanding hypotheses of adaptive radiation: hybrid swarm origins and temporal stages of adaptation. Using a combination of population genomics, transcriptomics, and genome-wide association mapping, we demonstrate that this microendemic adaptive radiation of novel trophic specialists on San Salvador Island, Bahamas experienced twice as much adaptive introgression as generalist populations on neighboring islands and that adaptive divergence occurred in stages. First, standing regulatory variation in genes associated with feeding behavior (prlh, cfap20, and rmi1) were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development (itga5, ext1, cyp26b1, and galr2) and finally the only de novo nonsynonymous substitution in an osteogenic transcription factor and oncogene (twist1) swept to fixation most recently. Our results demonstrate how ancient alleles maintained in distinct environmental refugia can be assembled into new adaptive combinations and provide a framework for reconstructing the spatiotemporal landscape of adaptation and speciation.
Rapid diversification often involves complex histories of gene flow that leave variable and conflicting signatures of evolutionary relatedness across the genome. Identifying the extent and source of variation in these evolutionary relationships can provide insight into the evolutionary mechanisms involved in rapid radiations. Here we compare the discordant evolutionary relationships associated with species phenotypes across 42 whole genomes from a sympatric adaptive radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas and several outgroup pupfish species in order to understand the rarity of these trophic specialists within the larger radiation of Cyprinodon. 82% of the genome depicts close evolutionary relationships among the San Salvador Island species reflecting their geographic proximity, but the vast majority of variants fixed between specialist species lie in regions with discordant topologies. Top candidate adaptive introgression regions include signatures of selective sweeps and adaptive introgression of genetic variation from a single population in the northwestern Bahamas into each of the specialist species. Hard selective sweeps of genetic variation on San Salvador Island contributed 5 times more to speciation of trophic specialists than adaptive introgression of Caribbean genetic variation; however, four of the 11 introgressed regions came from a single distant island and were associated with the primary axis of oral jaw divergence within the radiation. For example, standing variation in a proto-oncogene (ski) known to have effects on jaw size introgressed into one San Salvador Island specialist from an island 300 km away approximately 10 kya. The complex emerging picture of the origins of adaptive radiation on San Salvador Island indicates that multiple sources of genetic variation contributed to the adaptive phenotypes of novel trophic specialists on the island. Our findings suggest that a suite of factors, including rare adaptive introgression, may be necessary for adaptive radiation in addition to ecological opportunity.
The process of sympatric speciation in nature remains a fundamental unsolved problem. Cameroon crater lake cichlid radiations were long regarded as one of the most compelling examples; however, recent work showed that their origins were more complex than a single colonization event followed by isolation. Here, we performed a detailed investigation of the speciation history of a radiation of Coptodon cichlids from Lake Ejagham, Cameroon, using whole-genome sequencing data. The existence of the Lake Ejagham Coptodon radiation is remarkable as this 0.5 km lake offers limited scope for divergence across a shallow depth gradient, disruptive selection is currently weak, and the species are sexually monochromatic. We infer that Lake Ejagham was colonized by Coptodon cichlids soon after its formation 9,000 years ago, yet speciation occurred only in the last 1,000-2,000 years. We show that secondary gene flow from a nearby riverine species has been ongoing, into ancestral as well as extant lineages, and we identify and date river-to-lake admixture blocks. One block contains a cluster of olfactory receptor genes that introgressed near the time of the first speciation event and coincides with a higher overall rate of admixture. Olfactory signalling is a key component of mate choice and species recognition in cichlids. A functional role for this introgression event is consistent with previous findings that sexual isolation appears much stronger than ecological isolation in Ejagham Coptodon. We conclude that speciation in this radiation took place in sympatry, yet may have benefited from ongoing riverine gene flow.
Sympatric speciation illustrates how natural and sexual selection may create new species in isolation without geographic barriers. However, recent genomic reanalyses of classic examples of sympatric speciation reveal complex histories of secondary gene flow from outgroups into the radiation. In contrast, the rich theoretical literature on this process distinguishes among a diverse range of models based on simple genetic histories and different types of reproductive isolating barriers. Thus, there is a need to revisit how to connect theoretical models of sympatric speciation and their predictions to empirical case studies in the face of widespread gene flow. Here, theoretical differences among different types of sympatric speciation and speciation-with-gene-flow models are reviewed and genomic analyses for distinguishing which models apply to case studies based on the timing and function of adaptive introgression are proposed. Investigating whether secondary gene flow contributed to reproductive isolation is necessary to test whether predictions of theory are ultimately borne out in nature.
The use of large genomic data sets in phylogenetics has highlighted extensive topological variation across genes. Much of this discordance is assumed to result from biological processes. However, variation among gene trees can also be a consequence of systematic error driven by poor model fit, and the relative importance of biological vs. methodological factors in explaining gene tree variation is a major unresolved question. Using mitochondrial genomes to control for biological causes of gene tree variation, we estimate the extent of gene tree discordance driven by systematic error and employ posterior prediction to highlight the role of model fit in producing this discordance. We find that the amount of discordance among mitochondrial gene trees is similar to the amount of discordance found in other studies that assume only biological causes of variation. This similarity suggests that the role of systematic error in generating gene tree variation is underappreciated and critical evaluation of fit between assumed models and the data used for inference is important for the resolution of unresolved phylogenetic questions.
24Sympatric speciation illustrates how natural and sexual selection may create new species in 25 isolation without geographic barriers. However, recent genomic reanalyses of classic examples 26 of sympatric speciation have revealed complex histories of secondary gene flow. Thus, there is a 27 need to revisit how to connect the diverse theoretical models of sympatric speciation and their 28 predictions to empirical case studies in the face of widespread gene flow. We summarize 29 theoretical differences between sympatric speciation and speciation-with-gene-flow models and 30 propose genomic analyses for distinguishing which models apply to case studies based on the 31 timing and function of adaptive introgression. Investigating whether secondary gene flow 32 contributed to reproductive isolation is necessary to test whether predictions of theory are 33 ultimately borne out in nature. 34 35 36 37 38 39 40 41 42 43 44 45 46 3What is sympatric speciation? 47 As Mayr famously quipped, sympatric speciation is like the Lernean Hydra: "which grew two 48 new heads whenever one of its heads was cut off" (p. 451; [1]). The latest incarnation of this 49 phenomenon has occurred over the past decade: sympatric speciation now means two different 50 things to different research groups. 51In the classic definition, sympatric speciation represents the most extreme endpoint on 52 the divergence with gene flow continuum: panmictic gene flow and no initial divergence at the 53 start of speciation [2][3][4]. In the context of theoretical speciation models, this classic process of 54 sympatric speciation is the most difficult because the starting conditions involve no pre-existing 55 divergence, potentially tied with physical linkage, among loci involved in reproductive isolation. 56 Instead, linkage disequilibrium (see Glossary) must build up through time within a population 57 through the action of disruptive natural selection and strong assortative mating by ecotype, 58 despite the countervailing eroding force of recombination [5][6][7][8]. 59Recently, the definition of sympatric speciation has been expanded to focus more on 60 biogeographical context [9], in which the speciation process is defined as sympatric a) as long as 61 diverging populations are within 'cruising range' of each other and b) regardless of whether 62 secondary gene flow provided alleles contributing to reproductive isolating barriers in sympatry. 63Cruising range provides a practical empirical definition of gene flow between diverging 64 sympatric populations, allowing for some geographic or microallopatric population structure 65 (e.g. [10,11]). However, allowing for secondary gene flow of alleles contributing some or all of 66 the reproductive isolation between sympatric populations expands the definition of sympatric 67 speciation to include both hard and easy processes under one umbrella. Theoretical models show 68 4 that speciation is much easier from starting conditions that involve some level of initial 69 divergence and/or restricted gene flow, fo...
Genomic data has revealed complex histories of colonization and repeated gene flow previously unrecognized in some of the most celebrated examples of sympatric speciation and radiation. However, much of the evidence for secondary gene flow into these radiations comes from summary statistics calculated from sparse genomic sampling without knowledge of which specific genomic regions introgressed. This tells us little about how gene flow potentially influenced sympatric diversification. Here, we investigated whole genomes of Barombi Mbo crater lake cichlids for fine‐scale patterns of introgression with neighboring riverine cichlid populations. We found evidence of secondary gene flow into the radiation scattered across <0.24% of the genome; however, from our analyses, it is not clear if the functional diversity in these regions contributed to the ecological, sexual, and morphological diversity found in the lake. Unlike similar studies, we found no obvious candidate genes for adaptive introgression and we cannot rule out that secondary gene flow was predominantly neutral with respect to the diversification process. We also found evidence for differential assortment of ancestral polymorphisms found in riverine populations between sympatric sister species, suggesting the presence of an ancestral hybrid swarm. Although the history of gene flow and colonization is more complicated than previously assumed, the lack of compelling evidence for secondary gene flow's role in species diversification suggests that we should not yet rule out one of the most celebrated examples of sympatric speciation in nature without a more thorough investigation of the timing and functional role of each introgressed region.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.