Gene Loss and Parallel Evolution Contribute to Species Difference in Flower Color

Smith, Stacey D.; Rausher, Mark D.

doi:10.1093/molbev/msr109

Cited by 131 publications

(198 citation statements)

References 64 publications

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“…This QTL corresponds to the gene F3 0 5 0 h. Wessinger & Rausher [13] demonstrated using co-segregation and functional analyses that this gene is redundantly non-functional in P. barbatus and completely explains the difference in flower colour between the two species. Similar large effect flower colour QTLs have been reported frequently for adaptation to different pollinators between pairs of species within Aquilegia [35], Ipomopsis [15], Iris [14,17], Iochroma [36], Mimulus [9,37] and Petunia [10,18]. One partial explanation for this pattern is that many flower colour transitions involve deactivation of parts or all of the anthocyanin pathway, which can be accomplished by inactivating mutations in one or a few genes [10,13,36 -38].…”

Section: Discussion (A) Genetic Basis Of Pollination Syndrome Traits supporting

confidence: 58%

Identification of major quantitative trait loci underlying floral pollination syndrome divergence in Penstemon

Wessinger

Hileman

Rausher

2014

Phil. Trans. R. Soc. B

101

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Distinct floral pollination syndromes have emerged multiple times during the diversification of flowering plants. For example, in western North America, a hummingbird pollination syndrome has evolved more than 100 times, generally from within insect-pollinated lineages. The hummingbird syndrome is characterized by a suite of floral traits that attracts and facilitates pollen movement by hummingbirds, while at the same time discourages bee visitation. These floral traits generally include large nectar volume, red flower colour, elongated and narrow corolla tubes and reproductive organs that are exerted from the corolla. A handful of studies have examined the genetic architecture of hummingbird pollination syndrome evolution. These studies find that mutations of relatively large effect often explain increased nectar volume and transition to red flower colour. In addition, they suggest that adaptive suites of floral traits may often exhibit a high degree of genetic linkage, which could facilitate their fixation during pollination syndrome evolution. Here, we explore these emerging generalities by investigating the genetic basis of floral pollination syndrome divergence between two related Penstemon species with different pollination syndromes—bee-pollinated P. neomexicanus and closely related hummingbird-pollinated P. barbatus . In an F 2 mapping population derived from a cross between these two species, we characterized the effect size of genetic loci underlying floral trait divergence associated with the transition to bird pollination, as well as correlation structure of floral trait variation. We find the effect sizes of quantitative trait loci for adaptive floral traits are in line with patterns observed in previous studies, and find strong evidence that suites of floral traits are genetically linked. This linkage may be due to genetic proximity or pleiotropic effects of single causative loci. Interestingly, our data suggest that the evolution of floral traits critical for hummingbird pollination was not constrained by negative pleiotropy at loci that show co-localization for multiple traits.

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Section: Discussion (A) Genetic Basis Of Pollination Syndrome Traits supporting

confidence: 58%

Identification of major quantitative trait loci underlying floral pollination syndrome divergence in Penstemon

Wessinger

Hileman

Rausher

2014

Phil. Trans. R. Soc. B

101

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“…Although these assumptions are strengthened by parallels with ecological speciation [74], they ignore the genetic mechanisms underlying colour polymorphism, which may differ among species and constrain certain evolutionary outcomes. Different mutations can produce the same or similar pigment patterns in congeneric and even conspecific plants or animals, but each mutation may nevertheless have its own set of pleiotropic effects [29,75,76]. In plants, mutations that halt anthocyanin production may occur in structural genes for the flavonoid biochemical pathway or in transcription factor regions, with the latter presumed more tissue-specific and the former more deleterious for their plant-wide effects on the pathway by-products, including compounds that reduce physiological stress or herbivory [29].…”

Section: Discussionmentioning

confidence: 99%

Extrapolating from local ecological processes to genus-wide patterns in colour polymorphism in South AfricanProtea

Carlson

Holsinger

2015

Proc. R. Soc. B.

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Polymorphic traits are central to many fundamental discoveries in evolution, yet why they are found in some species and not others remains poorly understood. We use the African genus Protea-within which more than 40% of species have co-occurring pink and white floral colour morphs-to ask whether convergent evolution and ecological similarity could explain the genus-wide pattern of polymorphism. First, we identified environmental correlates of pink morph frequency across 28 populations of four species. Second, we determined whether the same correlates could predict species-level polymorphism and monomorphism across 31 species. We found that pink morph frequency increased with elevation in Protea repens and three section Exsertae species, increased eastward in P. repens, and increased with seed predation intensity in section Exsertae. For cross-species comparisons, populations of monomorphic pink species occurred at higher elevations than populations of monomorphic white species, and 18 polymorphic species spanned broader elevational gradients than 13 monomorphic species. These results suggest that divergent selection along elevational clines has repeatedly favoured polymorphism, and that more uniform selection in altitudinally restricted species may promote colour monomorphism. Our findings are, to our knowledge, the first to link selection acting within species to the presence and absence of colour polymorphism at broader phylogenetic scales.

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“…In this aspect, the inheritance mode resembles other typically irreversible transitions, such as the transition from outcrossing to selfing and from hermaphroditism to dioecy (69). In plants, for example, the shift from blue to red flowers in Andean Iochroma (Solanaceae) is irreversible; molecular studies suggest that loss of a gene encoding an enzyme in the anthocyanin pathway is needed for the transition, which limits the opportunity for later reversal to the ancestral state (69,70). Accordingly, the transition from induction to inheritance could, in principle, be made irreversible by a single gene mutation or gene loss in the induction pathway.…”

Section: Is the Transition To Inheritance Mode Irreversible And Convementioning

confidence: 99%

Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans

Whittle

Extavour

2017

Proc. Natl. Acad. Sci. U.S.A.

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In animals, primordial germ cells (PGCs) give rise to the germ lines, the cell lineages that produce sperm and eggs. PGCs form in embryogenesis, typically by one of two modes: a likely ancestral mode wherein germ cells are induced during embryogenesis by cell-cell signaling (induction) or a derived mechanism whereby germ cells are specified by using germ plasm-that is, maternally specified germ-line determinants (inheritance). The causes of the shift to germ plasm for PGC specification in some animal clades remain largely unknown, but its repeated convergent evolution raises the question of whether it may result from or confer an innate selective advantage. It has been hypothesized that the acquisition of germ plasm confers enhanced evolvability, resulting from the release of selective constraint on somatic gene networks in embryogenesis, thus leading to acceleration of an organism's protein-sequence evolution, particularly for genes expressed at early developmental stages, and resulting in high speciation rates in germ plasm-containing lineages (denoted herein as the "PGCspecification hypothesis"). Although that hypothesis, if supported, could have major implications for animal evolution, our recent large-scale coding-sequence analyses from vertebrates and invertebrates provided important examples of genera that do not support the hypothesis of liberated constraint under germ plasm. Here, we consider reasons why germ plasm might be neither a direct target of selection nor causally linked to accelerated animal evolution. We explore alternate scenarios that could explain the repeated evolution of germ plasm and propose potential consequences of the inheritance and induction modes to animal evolutionary biology.germ line | preformation | epigenesis | primordial germ cell | spandrel P rimordial germ cells (PGCs) are specialized cells located in sexual organs of animals. These cells are central to reproduction because they give rise to the germ lines and, ultimately, the sperm and eggs. The PGCs typically arise during early embryogenesis by one of two distinct modes: (i) induction, wherein germ cells are induced by cell-cell signaling pathways (also known as epigenesis); or (ii) inheritance, wherein germ cells are formed by using germ plasm (a specialized cytoplasm containing proteins and RNAs needed for PGC formation), that is, maternally generated germ-line determinants that are "preformed" before embryogenesis begins (also known as preformation) (1-3). The induction mode appears to be the more prevalent mode in animals and occurs in basally branching lineages, and thus is the hypothesized ancestral mechanism of PGC specification, whereas inheritance comprises the likely derived state (1) (Fig. 1) (see SI Appendix, section 1 on the less parsimonious scenario that induction is the derived mode). Induction has been inferred based on microscopic data from most animal clades studied to date and has been experimentally shown to occur in a diverse range of organisms, including mammals (Mus musculus) (4-8), salamanders (...

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Gene Loss and Parallel Evolution Contribute to Species Difference in Flower Color

Cited by 131 publications

References 64 publications

Identification of major quantitative trait loci underlying floral pollination syndrome divergence in Penstemon

Identification of major quantitative trait loci underlying floral pollination syndrome divergence in Penstemon

Extrapolating from local ecological processes to genus-wide patterns in colour polymorphism in South AfricanProtea

Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans

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