The Paradox Behind the Pattern of Rapid Adaptive Radiation: How Can the Speciation Process Sustain Itself Through an Early Burst?

Martin, Christopher H.; Richards, Emilie J.

doi:10.1146/annurev-ecolsys-110617-062443

Cited by 78 publications

(116 citation statements)

References 208 publications

(275 reference statements)

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“…Ecological speciation, i.e. speciation driven by differences in ecology, is considered the primary mode by which adaptive radiation can take place, and as various traits produce specific differences in ecology, certain traits are more strongly associated with the radiation process than others [3,11]. Therefore, it is vital to explain the effect of trait differences and how they contribute to species diversification, overall phenotypic disparity and ecological divergence.…”

Section: Introductionmentioning

confidence: 99%

Toxin expression in snake venom evolves rapidly with constant shifts in evolutionary rates

Barua

Mikheyev

2020

Proc. R. Soc. B.

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Key innovations provide ecological opportunity by enabling access to new resources, colonization of new environments, and are associated with adaptive radiation. The most well-known pattern associated with adaptive radiation is an early burst of phenotypic diversification. Venoms facilitate prey capture and are widely believed to be key innovations leading to adaptive radiation. However, few studies have estimated their evolutionary rate dynamics. Here, we test for patterns of adaptive evolution in venom gene expression data from 52 venomous snake species. By identifying shifts in tempo and mode of evolution along with models of phenotypic evolution, we show that snake venom exhibits the macroevolutionary dynamics expected of key innovations. Namely, all toxin families undergo shifts in their rates of evolution, likely in response to changes in adaptive optima. Furthermore, we show that rapid-pulsed evolution modelled as a Lévy process better fits snake venom evolution than conventional early burst or Ornstein–Uhlenbeck models. While our results support the idea of snake venom being a key innovation, the innovation of venom chemistry lacks clear mechanisms that would lead to reproductive isolation and thus adaptive radiation. Therefore, the extent to which venom directly influences the diversification process is still a matter of contention.

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Section: Introductionmentioning

confidence: 99%

Toxin expression in snake venom evolves rapidly with constant shifts in evolutionary rates

Barua

Mikheyev

2020

Proc. R. Soc. B.

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“…While the evidence is growing that hybridization can be a source of genetic variation that has facilitated adaptive radiations [5,10,[11][12][13][14][15][17][18][19]34] and has sometimes resulted in hybrid lineages that seeded more than one radiation [6,12], it remained obscure how hybridization could facilitate recurrent ARs long after the hybridization had taken place and in distant places. Our simulation study suggests that speciation and geographic isolation and subsequent secondary admixture of species or sub-lineages within a hybrid clade can enable geographic expansion and long-term maintenance of hybridization-induced genetic variation which exceeds mutation-selection-drift balance.…”

Section: Resultsmentioning

confidence: 99%

“…Growing empirical and theoretical evidence suggest that hybridization between genetically distant lineages can promote AR by assembling genes from distinct parental lineages into a wide array of novel genotypes [10][11][12][13][14][15][16][17][18][19] (the hybrid swarm origin hypothesis of AR [20]). However, at first consideration, such a contingency-dependent mechanism may seem unlikely to explain the repeated occurrence of AR within a lineage.…”

Section: Introductionmentioning

confidence: 99%

The propagation of admixture-derived adaptive radiation potential

Kagawa

Seehausen

2020

Proc. R. Soc. B.

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Adaptive radiations (ARs) frequently show remarkable repeatability where single lineages undergo multiple independent episodes of AR in distant places and long-separate time points. Genetic variation generated through hybridization between distantly related lineages can promote AR. This mechanism, however, requires rare coincidence in space and time between a hybridization event and opening of ecological opportunity, because hybridization generates large genetic variation only locally and it will persist only for a short period. Hence, hybridization seems unlikely to explain recurrent AR in the same lineage. Contrary to these expectations, our evolutionary computer simulations demonstrate that admixture variation can geographically spread and persist for long periods if the hybrid population becomes separated into isolated sub-lineages. Subsequent secondary hybridization of some of these can reestablish genetic polymorphisms from the ancestral hybridization in places far from the birthplace of the hybrid clade and long after the ancestral hybridization event. Consequently, simulations revealed conditions where exceptional genetic variation, once generated through a rare hybridization event, can facilitate multiple ARs exploiting ecological opportunities available at distant points in time and space.

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“…Adaptive variants associated with feeding behavior ( prlh; Fig 4A) and nasal protrusion ( tcf12 ; 99 th PIP percentile GWAS;Fig 4B;Data S8) originated in the northwestern Bahamas (New Providence Island, Exumas, and Cat Island) whereas adaptive introgression of variants associated with muscle development arrived from the southeastern Caribbean in the Dominican Republic ( cenpf, eya2; Fig 4A). This suggests that the extant SSI radiation of trophic specialists was reassembled from pools of ancient genetic variation contained in at least two distinct environmental refugia in other regions of the Caribbean, perhaps due to previous ephemeral adaptive radiations within these regions, thus connecting micro- and macroevolutionary-scale processes ( 30, 31 ).…”

Section: Main Textmentioning

confidence: 99%

“…Our results show that adaptive radiations can occupy expansive evolutionary spaces: spanning the existing radiation itself and the multitude of both past and present ephemeral pools of genetic variation that contributed to rapid diversification. Research into the broader spatiotemporal landscape of vertebrate radiations, including the hominin radiation ( 31 ), can provide clear answers regarding longstanding hypotheses about their origins and contributions to global patterns of biodiversity.…”

Section: Main Textmentioning

confidence: 99%

Major stages of vertebrate adaptive radiation are assembled from a disparate spatiotemporal landscape

Richards

McGirr²,

Wang³

et al. 2020

Preprint

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To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed 17 the spatial and temporal histories of genetic variants underlying major phenotypic axes of 18 diversification from the genomes of 202 Caribbean pupfishes. Ancient standing variation from 19 disparate spatial sources was reassembled into new combinations which are under strong 20 selection for adaptation to novel trophic niches on only a single island throughout the Caribbean. 21 This occurred in three stages: first, standing variation associated with feeding behavior swept, 22 103 7 which scale-eater candidate adaptive variants were significantly enriched, with relevant terms 104 corresponding to major axes of divergence in this radiation highlighted in bold (FDR < 0.01; full 105 list of terms with FDR < 0.05 in Table S4). 106 107 Even though both trophic specialists are endemic to SSI, we also found nearly all their 108 candidate adaptive variants to occur as standing genetic variation across the Caribbean 109 (molluscivore: 100%; scale-eater: 98%; Fig. 2A). Furthermore, nearly half these variants were 110 ancient and also found in Cualac or Megupsilon outgroups to Cyprinodon (41% and 55% of 111 scale-eater and molluscivore adaptive variants, respectively), which diverged over 5 Mya (22). 112 However, most adaptive variants did not show any evidence of selection in five other focal high- 113 coverage Caribbean generalist populations (only 2% and 6% of scale-eater and molluscivore 114 variants, respectively; Fig. S3) and strong linkage disequilibrium among adaptive variants in SSI 115 trophic specialists was not observed in these focal populations (Fig. 2B). Thus, novel trophic 116 specialists within a microendemic adaptive radiation were almost entirely assembled from 117 ancient standing genetic variation through strong selection for new adaptive combinations of 118 alleles. 119 Multiple lines of evidence suggest that more hybridization and adaptive introgression 120 took place in SSI populations than other Caribbean island populations, consistent with the 121 hypothesis that hybridization triggered adaptive radiation. First, the strongest signal of 122 introgression across the Caribbean was into the root node of the SSI radiation (Fig. 3B). Second, 123 trophic specialists on San Salvador experienced at least twice as much adaptive introgression as 124 other generalist populations across the Caribbean (P < 0.006; Fig. 3C). Third, based on 125 129 9 130 Fig. 3. A history of hybridization across the Caribbean. A) A summary map of adaptive 131 introgression into SSI trophic specialists from focal generalist populations across the Caribbean, 132 with thickness of arrows proportional to the number of outlier regions of the fd statistic. B) 133 149 (mediated through foraging behavior: scale-eating or snail-eating), trophic morphology, and 150 sexual communication signals. Based on both GO annotations of genes near candidate adaptive 151 variants and genome-wide association mapping (GWAS) in Caribbean pupfishes for ...

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The Paradox Behind the Pattern of Rapid Adaptive Radiation: How Can the Speciation Process Sustain Itself Through an Early Burst?

Cited by 78 publications

References 208 publications

Toxin expression in snake venom evolves rapidly with constant shifts in evolutionary rates

Toxin expression in snake venom evolves rapidly with constant shifts in evolutionary rates

The propagation of admixture-derived adaptive radiation potential

Major stages of vertebrate adaptive radiation are assembled from a disparate spatiotemporal landscape

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