A beak size locus in Darwin’s finches facilitated character displacement during a drought

Lamichhaney, Sangeet; Fan, Han; Berglund, J. Andrew; Wang, Chao; Almén, Markus Sällman; Webster, Matthew T.; Grant, B. Rosemary; Grant, Peter R.; Andersson, Leif

doi:10.1126/science.aad8786

Cited by 230 publications

(258 citation statements)

References 43 publications

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“…In the present study, the large differences in the principal toxin expression between NK-M and NK-T were most likely the result of directional selection, potentially due to local selective pressures and/or coevolution with distinct prey populations or species. Adaptive expression variations have been well documented in animals including venomous snakes, where the expression variability has been shown to account for the differences in venom function, particularly intraspecific venom function (Lamichhaney et al, 2015, 2016; Margres et al, 2016; Zhang & Reed, 2016). …”

Section: Resultsmentioning

confidence: 99%

Comparative venom gland transcriptomics ofNaja kaouthia(monocled cobra) from Malaysia and Thailand: elucidating geographical venom variation and insights into sequence novelty

Tan

Chanhome

et al. 2017

PeerJ

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BackgroundThe monocled cobra (Naja kaouthia) is a medically important venomous snake in Southeast Asia. Its venom has been shown to vary geographically in relation to venom composition and neurotoxic activity, indicating vast diversity of the toxin genes within the species. To investigate the polygenic trait of the venom and its locale-specific variation, we profiled and compared the venom gland transcriptomes of N. kaouthia from Malaysia (NK-M) and Thailand (NK-T) applying next-generation sequencing (NGS) technology.MethodsThe transcriptomes were sequenced on the Illumina HiSeq platform, assembled and followed by transcript clustering and annotations for gene expression and function. Pairwise or multiple sequence alignments were conducted on the toxin genes expressed. Substitution rates were studied for the major toxins co-expressed in NK-M and NK-T.Results and discussionThe toxin transcripts showed high redundancy (41–82% of the total mRNA expression) and comprised 23 gene families expressed in NK-M and NK-T, respectively (22 gene families were co-expressed). Among the venom genes, three-finger toxins (3FTxs) predominated in the expression, with multiple sequences noted. Comparative analysis and selection study revealed that 3FTxs are genetically conserved between the geographical specimens whilst demonstrating distinct differential expression patterns, implying gene up-regulation for selected principal toxins, or alternatively, enhanced transcript degradation or lack of transcription of certain traits. One of the striking features that elucidates the inter-geographical venom variation is the up-regulation of α-neurotoxins (constitutes ∼80.0% of toxin’s fragments per kilobase of exon model per million mapped reads (FPKM)), particularly the long-chain α-elapitoxin-Nk2a (48.3%) in NK-T but only 1.7% was noted in NK-M. Instead, short neurotoxin isoforms were up-regulated in NK-M (46.4%). Another distinct transcriptional pattern observed is the exclusively and abundantly expressed cytotoxin CTX-3 in NK-T. The findings suggested correlation with the geographical variation in proteome and toxicity of the venom, and support the call for optimising antivenom production and use in the region. Besides, the current study uncovered full and partial sequences of numerous toxin genes from N. kaouthia which have not been reported hitherto; these include N. kaouthia-specific l-amino acid oxidase (LAAO), snake venom serine protease (SVSP), cystatin, acetylcholinesterase (AChE), hyaluronidase (HYA), waprin, phospholipase B (PLB), aminopeptidase (AP), neprilysin, etc. Taken together, the findings further enrich the snake toxin database and provide deeper insights into the genetic diversity of cobra venom toxins.

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Section: Resultsmentioning

confidence: 99%

Comparative venom gland transcriptomics ofNaja kaouthia(monocled cobra) from Malaysia and Thailand: elucidating geographical venom variation and insights into sequence novelty

Tan

Chanhome

et al. 2017

PeerJ

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“…Both pygmy mice and dwarf rabbits show altered craniofacial development, characterized by shortened heads (Zhou et al 1995) (Figure 1). Interestingly, a recent study showed that HMGA2 is a major locus affecting craniofacial development (beak size) in Darwin's finches (Lamichhaney et al 2016), but in that case the phenotypic effect is likely caused by regulatory changes.…”

Section: Discussionmentioning

confidence: 99%

Dwarfism and Altered Craniofacial Development in Rabbits Is Caused by a 12.1 kb Deletion at the HMGA2 Locus

Carneiro

Archer

et al. 2017

Genetics

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The dwarf phenotype characterizes the smallest of rabbit breeds and is governed largely by the effects of a single dwarfing allele with an incompletely dominant effect on growth. Dwarf rabbits typically weigh under 1 kg and have altered craniofacial morphology. The dwarf allele is recessive lethal and dwarf homozygotes die within a few days of birth. The dwarf phenotype is expressed in heterozygous individuals and rabbits from dwarf breeds homozygous for the wild-type allele are normal, although smaller when compared to other breeds. Here, we show that the dwarf allele constitutes a 12.1 kb deletion overlapping the promoter region and first three exons of the HMGA2 gene leading to inactivation of this gene. HMGA2 has been frequently associated with variation in body size across species. Homozygotes for null alleles are viable in mice but not in rabbits and probably not in humans. RNA-sequencing analysis of rabbit embryos showed that very few genes (4-29 genes) were differentially expressed among the three HMGA2/dwarf genotypes, suggesting that dwarfism and inviability in rabbits are caused by modest changes in gene expression. Our results show that HMGA2 is critical for normal expression of IGF2BP2, which encodes an RNA-binding protein. Finally, we report a catalog of regions of elevated genetic differentiation between dwarf and normal-size rabbits, including LCORL-NCAPG, STC2, HOXD cluster, and IGF2BP2. Levels and patterns of genetic diversity at the LCORL-NCAPG locus further suggest that small size in dwarf breeds was enhanced by crosses with wild rabbits. Overall, our results imply that small size in dwarf rabbits results from a large effect, loss-of-function (LOF) mutation in HMGA2 combined with polygenic selection.

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“…Notably two variants of a gene (HMGA2) with major effects on beak size changed in frequency in the expected direction as a result of natural selection in 2004-2005 [56]. Less predictable are the effects of environmental extremes on evolution [57].…”

Section: Demography Of Birdsmentioning

confidence: 99%

Evolution caused by extreme events

Grant

Huey

et al. 2017

Phil. Trans. R. Soc. B

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195

172

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One contribution of 14 to a theme issue 'Behavioural, ecological and evolutionary responses to extreme climatic events'. Extreme events can be a major driver of evolutionary change over geological and contemporary timescales. Outstanding examples are evolutionary diversification following mass extinctions caused by extreme volcanism or asteroid impact. The evolution of organisms in contemporary time is typically viewed as a gradual and incremental process that results from genetic change, environmental perturbation or both. However, contemporary environments occasionally experience strong perturbations such as heat waves, floods, hurricanes, droughts and pest outbreaks. These extreme events set up strong selection pressures on organisms, and are small-scale analogues of the dramatic changes documented in the fossil record. Because extreme events are rare, almost by definition, they are difficult to study. So far most attention has been given to their ecological rather than to their evolutionary consequences. We review several case studies of contemporary evolution in response to two types of extreme environmental perturbations, episodic ( pulse) or prolonged (press). Evolution is most likely to occur when extreme events alter community composition. We encourage investigators to be prepared for evolutionary change in response to rare events during long-term field studies.This article is part of the themed issue 'Behavioural, ecological and evolutionary responses to extreme climatic events'.

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A beak size locus in Darwin’s finches facilitated character displacement during a drought

Cited by 230 publications

References 43 publications

Comparative venom gland transcriptomics ofNaja kaouthia(monocled cobra) from Malaysia and Thailand: elucidating geographical venom variation and insights into sequence novelty

Comparative venom gland transcriptomics ofNaja kaouthia(monocled cobra) from Malaysia and Thailand: elucidating geographical venom variation and insights into sequence novelty

Dwarfism and Altered Craniofacial Development in Rabbits Is Caused by a 12.1 kb Deletion at the HMGA2 Locus

Evolution caused by extreme events

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