Publications by authors named "Stephen H Montgomery"

33 Publications

Chromosome fusion affects genetic diversity and evolutionary turnover of functional loci, but consistently depends on chromosome size.

Mol Biol Evol 2021 Jun 19. Epub 2021 Jun 19.

School of Biological Sciences, University of Bristol Bristol - Life Sciences Building, Bristol, UK.

Major changes in chromosome number and structure are linked to a series of evolutionary phenomena, including intrinsic barriers to gene flow or suppression of recombination due to chromosomal rearrangements. However, chromosome rearrangements can also affect the fundamental dynamics of molecular evolution within populations by changing relationships between linked loci and altering rates of recombination. Here, we build chromosome-level assembly Eueides isabella and, together with a recent chromosome-level assembly of Dryas iulia, examine the evolutionary consequences of multiple chromosome fusions in Heliconius butterflies. These assemblies pinpoint fusion points on 10 of the 20 autosomal chromosomes and reveal striking differences in the characteristics of fused and unfused chromosomes. The ten smallest autosomes in D. iulia and E. isabella, which have each fused to a longer chromosome in Heliconius, have higher repeat and GC content, and longer introns than predicted by their chromosome length. When fused, these characteristics change to become more in line with chromosome length. The fusions also led to reduced diversity, which likely reflects increased background selection and selection against introgression between diverging populations, following a reduction in per-base recombination rate. We further show that chromosome size and fusion impact turnover rates of functional loci at a macroevolutionary scale. Together these results provide further evidence that chromosome fusion in Heliconius likely had dramatic effects on population level processes shaping rates of neutral and adaptive divergence. These effects may have impacted patterns of diversification in Heliconius, a classic example of an adaptive radiation.
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http://dx.doi.org/10.1093/molbev/msab185DOI Listing
June 2021

The Dryas iulia Genome Supports Multiple Gains of a W Chromosome from a B Chromosome in Butterflies.

Genome Biol Evol 2021 Jul;13(7)

School of Biological Sciences, University of Bristol, United Kingdom.

In butterflies and moths, which exhibit highly variable sex determination mechanisms, the homogametic Z chromosome is deeply conserved and is featured in many genome assemblies. The evolution and origin of the female W sex chromosome, however, remains mostly unknown. Previous studies have proposed that a ZZ/Z0 sex determination system is ancestral to Lepidoptera, and that W chromosomes may originate from sex-linked B chromosomes. Here, we sequence and assemble the female Dryas iulia genome into 32 highly contiguous ordered and oriented chromosomes, including the Z and W sex chromosomes. We then use sex-specific Hi-C, ATAC-seq, PRO-seq, and whole-genome DNA sequence data sets to test if features of the D. iulia W chromosome are consistent with a hypothesized B chromosome origin. We show that the putative W chromosome displays female-associated DNA sequence, gene expression, and chromatin accessibility to confirm the sex-linked function of the W sequence. In contrast with expectations from studies of homologous sex chromosomes, highly repetitive DNA content on the W chromosome, the sole presence of domesticated repetitive elements in functional DNA, and lack of sequence homology with the Z chromosome or autosomes is most consistent with a B chromosome origin for the W, although it remains challenging to rule out extensive sequence divergence. Synteny analysis of the D. iulia W chromosome with other female lepidopteran genome assemblies shows no homology between W chromosomes and suggests multiple, independent origins of the W chromosome from a B chromosome likely occurred in butterflies.
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http://dx.doi.org/10.1093/gbe/evab128DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8290107PMC
July 2021

An agent-based model clarifies the importance of functional and developmental integration in shaping brain evolution.

BMC Biol 2021 May 10;19(1):97. Epub 2021 May 10.

School of Biological Sciences, University of Bristol, Bristol, UK.

Background: Vertebrate brain structure is characterised not only by relative consistency in scaling between components, but also by many examples of divergence from these general trends.. Alternative hypotheses explain these patterns by emphasising either 'external' processes, such as coordinated or divergent selection, or 'internal' processes, like developmental coupling among brain regions. Although these hypotheses are not mutually exclusive, there is little agreement over their relative importance across time or how that importance may vary across evolutionary contexts.

Results: We introduce an agent-based model to simulate brain evolution in a 'bare-bones' system and examine dependencies between variables shaping brain evolution. We show that 'concerted' patterns of brain evolution do not, in themselves, provide evidence for developmental coupling, despite these terms often being treated as synonymous in the literature. Instead, concerted evolution can reflect either functional or developmental integration. Our model further allows us to clarify conditions under which such developmental coupling, or uncoupling, is potentially adaptive, revealing support for the maintenance of both mechanisms in neural evolution. Critically, we illustrate how the probability of deviation from concerted evolution depends on the cost/benefit ratio of neural tissue, which increases when overall brain size is itself under constraint.

Conclusions: We conclude that both developmentally coupled and uncoupled brain architectures can provide adaptive mechanisms, depending on the distribution of selection across brain structures, life history and costs of neural tissue. However, when constraints also act on overall brain size, heterogeneity in selection across brain structures will favour region specific, or mosaic, evolution. Regardless, the respective advantages of developmentally coupled and uncoupled brain architectures mean that both may persist in fluctuating environments. This implies that developmental coupling is unlikely to be a persistent constraint, but could evolve as an adaptive outcome to selection to maintain functional integration.
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http://dx.doi.org/10.1186/s12915-021-01024-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8111752PMC
May 2021

Neural divergence and hybrid disruption between ecologically isolated butterflies.

Proc Natl Acad Sci U S A 2021 02;118(6)

Smithsonian Tropical Research Institute, 0843-03092 Gamboa, Panama.

The importance of behavioral evolution during speciation is well established, but we know little about how this is manifest in sensory and neural systems. A handful of studies have linked specific neural changes to divergence in host or mate preferences associated with speciation. However, the degree to which brains are adapted to local environmental conditions, and whether this contributes to reproductive isolation between close relatives that have diverged in ecology, remains unknown. Here, we examine divergence in brain morphology and neural gene expression between closely related, but ecologically distinct, butterflies. Despite ongoing gene flow, sympatric species pairs within the complex are consistently separated across a gradient of open to closed forest and decreasing light intensity. By generating quantitative neuroanatomical data for 107 butterflies, we show that and clades have substantial shifts in brain morphology across their geographic range, with divergent structures clustered in the visual system. These neuroanatomical differences are mirrored by extensive divergence in neural gene expression. Differences in both neural morphology and gene expression are heritable, exceed expected rates of neutral divergence, and result in intermediate traits in first-generation hybrid offspring. Strong evidence of divergent selection implies local adaptation to distinct selective optima in each parental microhabitat, suggesting the intermediate traits of hybrids are poorly matched to either condition. Neural traits may therefore contribute to coincident barriers to gene flow, thereby helping to facilitate speciation.
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http://dx.doi.org/10.1073/pnas.2015102118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8017967PMC
February 2021

Pollen feeding in butterflies: the singular evolution of an adaptive suite.

Proc Biol Sci 2020 11 11;287(1938):20201304. Epub 2020 Nov 11.

School of Biological Science, University of Bristol, 24 Tyndall Avenue, Bristol UBS8 1TQ, UK.

Major evolutionary transitions can be triggered by behavioural novelty, and are often associated with 'adaptive suites', which involve shifts in multiple co-adapted traits subject to complex interactions. butterflies represent one such example, actively feeding on pollen, a behaviour unique among butterflies. Pollen feeding permits a prolonged reproductive lifespan, and co-occurs with a constellation of behavioural, neuroanatomical, life history, morphological and physiological traits that are absent in closely related, non-pollen-feeding genera. As a highly tractable system, supported by considerable ecological and genomic data, are an excellent model for investigating how behavioural innovation can trigger a cascade of adaptive shifts in multiple diverse, but interrelated, traits. Here, we synthesize current knowledge of pollen feeding in , and explore potential interactions between associated, putatively adaptive, traits. Currently, no physiological, morphological or molecular innovation has been explicitly linked to the origin of pollen feeding, and several hypothesized links between different aspects of biology remain poorly tested. However, resolving these uncertainties will contribute to our understanding of how behavioural innovations evolve and subsequently alter the evolutionary trajectories of diverse traits impacting resource acquisition, life history, senescence and cognition.
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http://dx.doi.org/10.1098/rspb.2020.1304DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7735275PMC
November 2020

Linking ecological specialisation to adaptations in butterfly brains and sensory systems.

Curr Opin Insect Sci 2020 12 23;42:55-60. Epub 2020 Sep 23.

School of Biological Sciences, University of Bristol, 24 Tyndall Avenue, Bristol, BS8 1TQ, UK. Electronic address:

Butterflies display incredible ecological and behavioural diversity. As such, they have been subject to intense study since the birth of evolutionary biology. However, with some possible exceptions, they are underused models in comparative and functional neurobiology. We highlight a series of areas, spanning sensory ecology to cognition, in which butterflies are particularly promising systems for investigating the neurobiological basis for behavioural or ecological variation. These fields benefit from a history of molecular and quantitative genetics, and basic comparative neuroanatomy, but these strands of research are yet to be widely integrated. We discuss areas for potential growth and argue that new experimental techniques, growing genomic resources, and tools for functional genetics will accelerate the use of butterflies in neurobiology.
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http://dx.doi.org/10.1016/j.cois.2020.09.002DOI Listing
December 2020

Heliconiini butterflies can learn time-dependent reward associations.

Biol Lett 2020 09 23;16(9):20200424. Epub 2020 Sep 23.

Smithsonian Tropical Research Institute, Gamboa, Panama.

For many pollinators, flowers provide predictable temporal schedules of resource availability, meaning an ability to learn time-dependent information could be widely beneficial. However, this ability has only been demonstrated in a handful of species. Observations of butterflies suggest that they may have an ability to form time-dependent foraging preferences. are unique among butterflies in actively collecting pollen, a dietary behaviour linked to spatio-temporally faithful 'trap-line' foraging. Time dependency of foraging preferences is hypothesized to allow to exploit temporal predictability in alternative pollen resources. Here, we provide the first experimental evidence in support of this hypothesis, demonstrating that can learn opposing colour preferences in two time periods. This shift in preference is robust to the order of presentation, suggesting that preference is tied to the time of day and not due to ordinal or interval learning. However, this ability is not limited to , as previously hypothesized, but also present in a related genus of non-pollen feeding butterflies. This demonstrates time learning likely pre-dates the origin of pollen feeding and may be prevalent across butterflies with less specialized foraging behaviours.
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http://dx.doi.org/10.1098/rsbl.2020.0424DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7532716PMC
September 2020

Visual mate preference evolution during butterfly speciation is linked to neural processing genes.

Nat Commun 2020 09 21;11(1):4763. Epub 2020 Sep 21.

Division of Evolutionary Biology, LMU, Munich, Germany.

Many animal species remain separate not because their individuals fail to produce viable hybrids but because they "choose" not to mate. However, we still know very little of the genetic mechanisms underlying changes in these mate preference behaviours. Heliconius butterflies display bright warning patterns, which they also use to recognize conspecifics. Here, we couple QTL for divergence in visual preference behaviours with population genomic and gene expression analyses of neural tissue (central brain, optic lobes and ommatidia) across development in two sympatric Heliconius species. Within a region containing 200 genes, we identify five genes that are strongly associated with divergent visual preferences. Three of these have previously been implicated in key components of neural signalling (specifically an ionotropic glutamate receptor and two regucalcins), and overall our candidates suggest shifts in behaviour involve changes in visual integration or processing. This would allow preference evolution without altering perception of the wider environment.
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http://dx.doi.org/10.1038/s41467-020-18609-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7506007PMC
September 2020

Bias and Misrepresentation of Science Undermines Productive Discourse on Animal Welfare Policy: A Case Study.

Animals (Basel) 2020 Jun 29;10(7). Epub 2020 Jun 29.

School of Biological Sciences, University of Bristol, Bristol, BS8 1TQ, UK.

Reliable scientific knowledge is crucial for informing legislative, regulatory, and policy decisions in a variety of areas. To that end, scientific reviews of topical issues can be invaluable tools for informing productive discourse and decision-making, assuming these reviews represent the target body of scientific knowledge as completely, accurately, and objectively as possible. Unfortunately, not all reviews live up to this standard. As a case in point, Marino et al.'s [1] review regarding the welfare of killer whales in captivity contains methodological flaws and misrepresentations of the scientific literature, including problematic referencing, overinterpretation of the data, misleading word choice, and biased argumentation. These errors and misrepresentations undermine the authors' conclusions and make it impossible to determine the true state of knowledge of the relevant issues. To achieve the goal of properly informing public discourse and policy on this and other issues, it is imperative that scientists and science communicators strive for higher standards of analysis, argumentation, and objectivity, in order to clearly communicate what is known, what is not known, what conclusions are supported by the data, and where we are lacking the data necessary to draw reliable conclusions.
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http://dx.doi.org/10.3390/ani10071118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7401611PMC
June 2020

Are brain weights estimated from scaling relationships suitable for comparative studies of animal cognition?

Anim Cogn 2019 Nov 21;22(6):1191-1195. Epub 2019 Aug 21.

Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK.

What is the cognitive significance of variation in brain size? This question is simply put, but hard to answer, and remains one of the most enduring questions in comparative ethology. Understanding the causative links between variation in brain size and structure, and cognition requires reliable data on both neural and behavioral traits. A recent study by Horschler et al. (Anim Cogn 22(2):187-198, 2019) demonstrated the potential of citizen science and domestic dogs to provide unprecedented behavioral datasets that can be used to tackle this question. However, data on brain weight is harder to source. To test the link between performance in various cognitive tasks and variation in brain size, the authors instead relied on data for body weight, which was transformed into 'estimated brain weight' using the allometric scaling relationship between brain and body size, an approach that can be found in other papers which lack sufficient neuroanatomical data. Here, I describe some probable limitations of this approach and suggest that such transformations provide no benefit to the analyses and should be avoided.
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http://dx.doi.org/10.1007/s10071-019-01300-2DOI Listing
November 2019

Proportional versus relative size as metrics in human brain evolution.

Proc Natl Acad Sci U S A 2019 01 17;116(1):3-4. Epub 2018 Dec 17.

Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom.

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http://dx.doi.org/10.1073/pnas.1817200116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6320533PMC
January 2019

Genetics of Cerebellar and Neocortical Expansion in Anthropoid Primates: A Comparative Approach.

Brain Behav Evol 2017 6;89(4):274-285. Epub 2017 Jul 6.

Department of Genetics, Evolution and Environment, University College London, London, UK.

What adaptive changes in brain structure and function underpin the evolution of increased cognitive performance in humans and our close relatives? Identifying the genetic basis of brain evolution has become a major tool in answering this question. Numerous cases of positive selection, altered gene expression or gene duplication have been identified that may contribute to the evolution of the neocortex, which is widely assumed to play a predominant role in cognitive evolution. However, the components of the neocortex co-evolve with other functionally interdependent regions of the brain, most notably in the cerebellum. The cerebellum is linked to a range of cognitive tasks and expanded rapidly during hominoid evolution. Here we present data that suggest that, across anthropoid primates, protein-coding genes with known roles in cerebellum development were just as likely to be targeted by selection as genes linked to cortical development. Indeed, based on currently available gene ontology data, protein-coding genes with known roles in cerebellum development are more likely to have evolved adaptively during hominoid evolution. This is consistent with phenotypic data suggesting an accelerated rate of cerebellar expansion in apes that is beyond that predicted from scaling with the neocortex in other primates. Finally, we present evidence that the strength of selection on specific genes is associated with variation in the volume of either the neocortex or the cerebellum, but not both. This result provides preliminary evidence that co-variation between these brain components during anthropoid evolution may be at least partly regulated by selection on independent loci, a conclusion that is consistent with recent intraspecific genetic analyses and a mosaic model of brain evolution that predicts adaptive evolution of brain structure.
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http://dx.doi.org/10.1159/000477432DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5637284PMC
April 2018

Evidence of a Conserved Molecular Response to Selection for Increased Brain Size in Primates.

Genome Biol Evol 2017 Mar;9(3):700-713

Wayne State University School of Medicine, Center for Molecular Medicine and Genetics, Detroit, Michigan, Detroit, MI.

The adaptive significance of human brain evolution has been frequently studied through comparisons with other primates. However, the evolution of increased brain size is not restricted to the human lineage but is a general characteristic of primate evolution. Whether or not these independent episodes of increased brain size share a common genetic basis is unclear. We sequenced and de novo assembled the transcriptome from the neocortical tissue of the most highly encephalized nonhuman primate, the tufted capuchin monkey (Cebus apella). Using this novel data set, we conducted a genome-wide analysis of orthologous brain-expressed protein coding genes to identify evidence of conserved gene-phenotype associations and species-specific adaptations during three independent episodes of brain size increase. We identify a greater number of genes associated with either total brain mass or relative brain size across these six species than show species-specific accelerated rates of evolution in individual large-brained lineages. We test the robustness of these associations in an expanded data set of 13 species, through permutation tests and by analyzing how genome-wide patterns of substitution co-vary with brain size. Many of the genes targeted by selection during brain expansion have glutamatergic functions or roles in cell cycle dynamics. We also identify accelerated evolution in a number of individual capuchin genes whose human orthologs are associated with human neuropsychiatric disorders. These findings demonstrate the value of phenotypically informed genome analyses, and suggest at least some aspects of human brain evolution have occurred through conserved gene-phenotype associations. Understanding these commonalities is essential for distinguishing human-specific selection events from general trends in brain evolution.
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http://dx.doi.org/10.1093/gbe/evx028DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5381557PMC
March 2017

Brain evolution and development: adaptation, allometry and constraint.

Proc Biol Sci 2016 09;283(1838)

Evolutionary Anthropology Research Group, Durham University, Dawson Building, South Road, Durham DH1 3LE, UK.

Phenotypic traits are products of two processes: evolution and development. But how do these processes combine to produce integrated phenotypes? Comparative studies identify consistent patterns of covariation, or allometries, between brain and body size, and between brain components, indicating the presence of significant constraints limiting independent evolution of separate parts. These constraints are poorly understood, but in principle could be either developmental or functional. The developmental constraints hypothesis suggests that individual components (brain and body size, or individual brain components) tend to evolve together because natural selection operates on relatively simple developmental mechanisms that affect the growth of all parts in a concerted manner. The functional constraints hypothesis suggests that correlated change reflects the action of selection on distributed functional systems connecting the different sub-components, predicting more complex patterns of mosaic change at the level of the functional systems and more complex genetic and developmental mechanisms. These hypotheses are not mutually exclusive but make different predictions. We review recent genetic and neurodevelopmental evidence, concluding that functional rather than developmental constraints are the main cause of the observed patterns.
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http://dx.doi.org/10.1098/rspb.2016.0433DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5031648PMC
September 2016

Inferring regulatory change from gene expression: the confounding effects of tissue scaling.

Mol Ecol 2016 10 15;25(20):5114-5128. Epub 2016 Sep 15.

Department of Genetics, Evolution and Environment, University College London, London, WC1E 6BT, UK.

Comparative studies of gene expression are often designed with the aim of identifying regulatory changes associated with phenotypic variation. In recent years, large-scale transcriptome sequencing methods have increasingly been applied to nonmodel organisms to ask important ecological or evolutionary questions. Although experimental design varies, many of these studies have been based on RNA libraries obtained from heterogeneous tissue samples, for example homogenized whole bodies. Comparisons between groups of samples that vary in tissue composition can introduce sufficient variation in RNA abundance to produce patterns of differential expression that are mistakenly interpreted as evidence of regulatory differences. Here, we present a simple model that demonstrates this effect. The model describes the relationship between transcript abundance and tissue composition in a two-tissue system, and how this relationship varies under different scaling relationships. Using a range of biologically realistic variables, including real biological examples, to parameterize the model we highlight the potentially severe influence of tissue scaling on relative transcript abundance. We use these results to identify key aspects of experimental design and analysis that can help to limit the influence of tissue scaling on the inference of regulatory difference from comparative studies of gene expression.
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http://dx.doi.org/10.1111/mec.13824DOI Listing
October 2016

Brain composition in Heliconius butterflies, posteclosion growth and experience-dependent neuropil plasticity.

J Comp Neurol 2016 Jun 4;524(9):1747-69. Epub 2016 Apr 4.

Department of Neuroscience, Psychology and Behaviour, University of Leicester, Leicester, UK.

Behavioral and sensory adaptations are often reflected in the differential expansion of brain components. These volumetric differences represent changes in cell number, size, and/or connectivity, which may denote changes in the functional and evolutionary relationships between different brain regions, and between brain composition and behavioral ecology. Here we describe the brain composition of two species of Heliconius butterflies, a long-standing study system for investigating ecological adaptation and speciation. We confirm a previous report of a striking volumetric expansion of the mushroom body, and explore patterns of differential posteclosion and experience-dependent plasticity between different brain regions. This analysis uncovers age- and experience-dependent posteclosion mushroom body growth comparable to that in foraging Hymenoptera, but also identifies plasticity in several other neuropils. An interspecific analysis indicates that Heliconius display a remarkably large investment in mushroom bodies for a lepidopteran, and indeed rank highly compared to other insects. Our analyses lay the foundation for future comparative and experimental analyses that will establish Heliconius as a valuable case study in evolutionary neurobiology.
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http://dx.doi.org/10.1002/cne.23993DOI Listing
June 2016

Phylogenetic Analysis Supports a Link between DUF1220 Domain Number and Primate Brain Expansion.

Genome Biol Evol 2015 Jun 25;7(8):2083-8. Epub 2015 Jun 25.

Department of Genetics, Evolution & Environment, University College London, United Kingdom

The expansion of DUF1220 domain copy number during human evolution is a dramatic example of rapid and repeated domain duplication. Although patterns of expression, homology, and disease associations suggest a role in cortical development, this hypothesis has not been robustly tested using phylogenetic methods. Here, we estimate DUF1220 domain counts across 12 primate genomes using a nucleotide Hidden Markov Model. We then test a series of hypotheses designed to examine the potential evolutionary significance of DUF1220 copy number expansion. Our results suggest a robust association with brain size, and more specifically neocortex volume. In contradiction to previous hypotheses, we find a strong association with postnatal brain development but not with prenatal brain development. Our results provide further evidence of a conserved association between specific loci and brain size across primates, suggesting that human brain evolution may have occurred through a continuation of existing processes.
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http://dx.doi.org/10.1093/gbe/evv122DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4558844PMC
June 2015

Sexual selection drives evolution and rapid turnover of male gene expression.

Proc Natl Acad Sci U S A 2015 Apr 23;112(14):4393-8. Epub 2015 Mar 23.

Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom.

The profound and pervasive differences in gene expression observed between males and females, and the unique evolutionary properties of these genes in many species, have led to the widespread assumption that they are the product of sexual selection and sexual conflict. However, we still lack a clear understanding of the connection between sexual selection and transcriptional dimorphism, often termed sex-biased gene expression. Moreover, the relative contribution of sexual selection vs. drift in shaping broad patterns of expression, divergence, and polymorphism remains unknown. To assess the role of sexual selection in shaping these patterns, we assembled transcriptomes from an avian clade representing the full range of sexual dimorphism and sexual selection. We use these species to test the links between sexual selection and sex-biased gene expression evolution in a comparative framework. Through ancestral reconstruction of sex bias, we demonstrate a rapid turnover of sex bias across this clade driven by sexual selection and show it to be primarily the result of expression changes in males. We use phylogenetically controlled comparative methods to demonstrate that phenotypic measures of sexual selection predict the proportion of male-biased but not female-biased gene expression. Although male-biased genes show elevated rates of coding sequence evolution, consistent with previous reports in a range of taxa, there is no association between sexual selection and rates of coding sequence evolution, suggesting that expression changes may be more important than coding sequence in sexual selection. Taken together, our results highlight the power of sexual selection to act on gene expression differences and shape genome evolution.
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http://dx.doi.org/10.1073/pnas.1501339112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4394296PMC
April 2015

Variation in promiscuity and sexual selection drives avian rate of Faster-Z evolution.

Mol Ecol 2015 Mar;24(6):1218-35

Department of Zoology, Edward Grey Institute, University of Oxford, Oxford, OX1 3PS, UK; Department of Genetics, Evolution and Environment, University College London, London, WC1E 6BT, UK.

Higher rates of coding sequence evolution have been observed on the Z chromosome relative to the autosomes across a wide range of species. However, despite a considerable body of theory, we lack empirical evidence explaining variation in the strength of the Faster-Z Effect. To assess the magnitude and drivers of Faster-Z Evolution, we assembled six de novo transcriptomes, spanning 90 million years of avian evolution. Our analysis combines expression, sequence and polymorphism data with measures of sperm competition and promiscuity. In doing so, we present the first empirical evidence demonstrating the positive relationship between Faster-Z Effect and measures of promiscuity, and therefore variance in male mating success. Our results from multiple lines of evidence indicate that selection is less effective on the Z chromosome, particularly in promiscuous species, and that Faster-Z Evolution in birds is due primarily to genetic drift. Our results reveal the power of mating system and sexual selection in shaping broad patterns in genome evolution.
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http://dx.doi.org/10.1111/mec.13113DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4737241PMC
March 2015

SWAMP: Sliding Window Alignment Masker for PAML.

Evol Bioinform Online 2014 1;10:197-204. Epub 2014 Dec 1.

Department of Genetics, Evolution and Environment, University College London, London, United Kingdom.

With the greater availability of genetic data, large genome-wide scans for positive selection increasingly incorporate data from a range of sources. These data sets may be derived from different sequencing methods, each of which has potential sources of error. Sequencing errors, compounded by alignment errors, greatly increase the number of false positives in tests for adaptive evolution. Genome-wide analyses often fail to fully address these issues or to provide sufficient detail on postalignment masking/filtering. Here, we introduce a Sliding Window Alignment Masker for Phylogenetic Analysis by Maximum Likelihood (SWAMP) that scans multiple-sequence alignments for short regions enriched with unreasonably high rates of nonsynonymous substitutions caused, for example, by sequence or alignment errors. SWAMP prevents their inclusion in downstream evolutionary analyses and therefore increases the reliability of downstream analyses. It is able to effectively mask short stretches of erroneous sequence, particularly prevalent in low-coverage genomes, which may not be detected by existing methods based on filtering by sitewise conservation or alignment confidence. SWAMP offers a flexible masking approach, and the user can apply different masking regimens to specific branches or sequences in the phylogeny allowing the stringency of masking to vary according to branch length, expected divergence levels, or assembly quality. We exemplify SWAMPs effectiveness on a dataset of 6,379 protein-coding genes from primate species, including data of variable quality. Full reporting of the software parameters will further improve the reproducibility of genome-wide analyses, as well as reduce false-positive rates.
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http://dx.doi.org/10.4137/EBO.S18193DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4251194PMC
December 2014

Brain composition in Godyris zavaleta, a diurnal butterfly, Reflects an increased reliance on olfactory information.

J Comp Neurol 2015 Apr 30;523(6):869-91. Epub 2014 Dec 30.

Department of Genetics, Evolution & Environment, University College London, London, UK, WC1E 6BT.

Interspecific comparisons of brain structure can inform our functional understanding of brain regions, identify adaptations to species-specific ecologies, and explore what constrains adaptive changes in brain structure, and coevolution between functionally related structures. The value of such comparisons is enhanced when the species considered have known ecological differences. The Lepidoptera have long been a favored model in evolutionary biology, but to date descriptions of brain anatomy have largely focused on a few commonly used neurobiological model species. We describe the brain of Godyris zavaleta (Ithomiinae), a member of a subfamily of Neotropical butterflies with enhanced reliance on olfactory information. We demonstrate for the first time the presence of sexually dimorphic glomeruli within a distinct macroglomerular complex (MGC) in the antennal lobe of a diurnal butterfly. This presents a striking convergence with the well-known moth MGC, prompting a discussion of the potential mechanisms behind the independent evolution of specialized glomeruli. Interspecific analyses across four Lepidoptera further show that the relative size of sensory neuropils closely mirror interspecific variation in sensory ecology, with G. zavaleta displaying levels of sensory investment intermediate between the diurnal monarch butterfly (Danaus plexippus), which invests heavily in visual neuropil, and night-flying moths, which invest more in olfactory neuropil. We identify several traits that distinguish butterflies from moths, and several that distinguish D. plexippus and G. zavaleta. Our results illustrate that ecological selection pressures mold the structure of invertebrate brains, and exemplify how comparative analyses across ecologically divergent species can illuminate the functional significance of variation in brain structure.
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http://dx.doi.org/10.1002/cne.23711DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4354442PMC
April 2015

Independent stratum formation on the avian sex chromosomes reveals inter-chromosomal gene conversion and predominance of purifying selection on the W chromosome.

Evolution 2014 Nov 29;68(11):3281-95. Epub 2014 Aug 29.

Department of Zoology, Edward Grey Institute, University of Oxford, Oxford, OX1 3PS, United Kingdom; Department of Genetics, Evolution and Environment, University College, London, London, WC1E 6BT, United Kingdom.

We used a comparative approach spanning three species and 90 million years to study the evolutionary history of the avian sex chromosomes. Using whole transcriptomes, we assembled the largest cross-species dataset of W-linked coding content to date. Our results show that recombination suppression in large portions of the avian sex chromosomes has evolved independently, and that long-term sex chromosome divergence is consistent with repeated and independent inversions spreading progressively to restrict recombination. In contrast, over short-term periods we observe heterogeneous and locus-specific divergence. We also uncover four instances of gene conversion between both highly diverged and recently evolved gametologs, suggesting a complex mosaic of recombination suppression across the sex chromosomes. Lastly, evidence from 16 gametologs reveal that the W chromosome is evolving with a significant contribution of purifying selection, consistent with previous findings that W-linked genes play an important role in encoding sex-specific fitness.
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http://dx.doi.org/10.1111/evo.12493DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4278454PMC
November 2014

Microcephaly genes evolved adaptively throughout the evolution of eutherian mammals.

BMC Evol Biol 2014 Jun 5;14:120. Epub 2014 Jun 5.

Department Genetics, Evolution & Environment, University College London, Gower Street, London WC1E 6BT, UK.

Background: Genes associated with the neurodevelopmental disorder microcephaly display a strong signature of adaptive evolution in primates. Comparative data suggest a link between selection on some of these loci and the evolution of primate brain size. Whether or not either positive selection or this phenotypic association are unique to primates is unclear, but recent studies in cetaceans suggest at least two microcephaly genes evolved adaptively in other large brained mammalian clades.

Results: Here we analyse the evolution of seven microcephaly loci, including three recently identified loci, across 33 eutherian mammals. We find extensive evidence for positive selection having acted on the majority of these loci not just in primates but also across non-primate mammals. Furthermore, the patterns of selection in major mammalian clades are not significantly different. Using phylogenetically corrected comparative analyses, we find that the evolution of two microcephaly loci, ASPM and CDK5RAP2, are correlated with neonatal brain size in Glires and Euungulata, the two most densely sampled non-primate clades.

Conclusions: Together with previous results, this suggests that ASPM and CDK5RAP2 may have had a consistent role in the evolution of brain size in mammals. Nevertheless, several limitations of currently available data and gene-phenotype tests are discussed, including sparse sampling across large evolutionary distances, averaging gene-wide rates of evolution, potential phenotypic variation and evolutionary reversals. We discuss the implications of our results for studies of the genetic basis of brain evolution, and explicit tests of gene-phenotype hypotheses.
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http://dx.doi.org/10.1186/1471-2148-14-120DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4055943PMC
June 2014

ASPM and mammalian brain evolution: a case study in the difficulty in making macroevolutionary inferences about gene-phenotype associations.

Proc Biol Sci 2014 Mar 22;281(1778):20131743. Epub 2014 Jan 22.

Department of Genetics, Evolution and Environment, University College London, , London, UK, Department of Zoology, University of Cambridge, , Cambridge, UK, Department of Anthropology, University of Durham, , Durham, UK.

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http://dx.doi.org/10.1098/rspb.2013.1743DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3906929PMC
March 2014

The evolutionary history of cetacean brain and body size.

Evolution 2013 Nov 23;67(11):3339-53. Epub 2013 Jul 23.

Department of Zoology, University of Cambridge, Downing Street, Cambridge, United Kingdom.

Cetaceans rival primates in brain size relative to body size and include species with the largest brains and biggest bodies to have ever evolved. Cetaceans are remarkably diverse, varying in both phenotypes by several orders of magnitude, with notable differences between the two extant suborders, Mysticeti and Odontoceti. We analyzed the evolutionary history of brain and body mass, and relative brain size measured by the encephalization quotient (EQ), using a data set of extinct and extant taxa to capture temporal variation in the mode and direction of evolution. Our results suggest that cetacean brain and body mass evolved under strong directional trends to increase through time, but decreases in EQ were widespread. Mysticetes have significantly lower EQs than odontocetes due to a shift in brain:body allometry following the divergence of the suborders, caused by rapid increases in body mass in Mysticeti and a period of body mass reduction in Odontoceti. The pattern in Cetacea contrasts with that in primates, which experienced strong trends to increase brain mass and relative brain size, but not body mass. We discuss what these analyses reveal about the convergent evolution of large brains, and highlight that until recently the most encephalized mammals were odontocetes, not primates.
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http://dx.doi.org/10.1111/evo.12197DOI Listing
November 2013

Primate brains, the 'island rule' and the evolution of Homo floresiensis.

J Hum Evol 2013 Dec 14;65(6):750-60. Epub 2013 Oct 14.

Department of Genetics, Evolution and Environment, University College London, Gower Street, London WC1E 6BT, United Kingdom. Electronic address:

The taxonomic status of the small bodied hominin, Homo floresiensis, remains controversial. One contentious aspect of the debate concerns the small brain size estimated for specimen LB1 (Liang Bua 1). Based on intraspecific mammalian allometric relationships between brain and body size, it has been argued that the brain of LB1 is too small for its body mass and is therefore likely to be pathological. The relevance and general applicability of these scaling rules has, however, been challenged, and it is not known whether highly encephalized primates adapt to insular habitats in a consistent manner. Here, an analysis of brain and body size evolution in seven extant insular primates reveals that although insular primates follow the 'island rule', having consistently reduced body masses compared with their mainland relatives, neither brain mass nor relative brain size follow similar patterns, contrary to expectations that energetic constraints will favour decreased relative brain size. Brain:body scaling relationships previously used to assess the plausibility of dwarfism in H. floresiensis tend to underestimate body masses of insular primates. In contrast, under a number of phylogenetic scenarios, the evolution of brain and body mass in H. floresiensis is consistent with patterns observed in other insular primates.
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http://dx.doi.org/10.1016/j.jhevol.2013.08.006DOI Listing
December 2013

Insights into hominid evolution from the gorilla genome sequence.

Nature 2012 Mar 7;483(7388):169-75. Epub 2012 Mar 7.

Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton CB10 1SA, UK.

Gorillas are humans' closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human-chimpanzee and human-chimpanzee-gorilla speciation events at approximately 6 and 10 million years ago. In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.
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http://dx.doi.org/10.1038/nature10842DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3303130PMC
March 2012

Evolution of ASPM is associated with both increases and decreases in brain size in primates.

Evolution 2012 Mar 1;66(3):927-932. Epub 2011 Dec 1.

Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, United Kingdom E-mail:

A fundamental trend during primate evolution has been the expansion of brain size. However, this trend was reversed in the Callitrichidae (marmosets and tamarins), which have secondarily evolved smaller brains associated with a reduction in body size. The recent pursuit of the genetic basis of brain size evolution has largely focused on episodes of brain expansion, but new insights may be gained by investigating episodes of brain size reduction. Previous results suggest two genes (ASPM and CDK5RAP2) associated with microcephaly, a human neurodevelopmental disorder, may have an evolutionary function in primate brain expansion. Here we use new sequences encoding key functional domains from 12 species of callitrichids to show that positive selection has acted on ASPM across callitrichid evolution and the rate of ASPM evolution is significantly negatively correlated with callitrichid brain size, whereas the evolution of CDK5RAP2 shows no correlation with brain size. Our findings strongly suggest that ASPM has a previously unsuspected role in the evolution of small brains in primates. ASPM is therefore intimately linked to both evolutionary increases and decreases in brain size in anthropoids and is a key target for natural selection acting on brain size.
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http://dx.doi.org/10.1111/j.1558-5646.2011.01487.xDOI Listing
March 2012

Phylogeny and adaptive evolution of the brain-development gene microcephalin (MCPH1) in cetaceans.

BMC Evol Biol 2011 Apr 14;11:98. Epub 2011 Apr 14.

Department of Biology, University of California, Riverside, 92521, USA.

Background: Representatives of Cetacea have the greatest absolute brain size among animals, and the largest relative brain size aside from humans. Despite this, genes implicated in the evolution of large brain size in primates have yet to be surveyed in cetaceans.

Results: We sequenced ~1240 basepairs of the brain development gene microcephalin (MCPH1) in 38 cetacean species. Alignments of these data and a published complete sequence from Tursiops truncatus with primate MCPH1 were utilized in phylogenetic analyses and to estimate ω (rate of nonsynonymous substitution/rate of synonymous substitution) using site and branch models of molecular evolution. We also tested the hypothesis that selection on MCPH1 was correlated with brain size in cetaceans using a continuous regression analysis that accounted for phylogenetic history. Our analyses revealed widespread signals of adaptive evolution in the MCPH1 of Cetacea and in other subclades of Mammalia, however, there was not a significant positive association between ω and brain size within Cetacea.

Conclusion: In conjunction with a recent study of Primates, we find no evidence to support an association between MCPH1 evolution and the evolution of brain size in highly encephalized mammalian species. Our finding of significant positive selection in MCPH1 may be linked to other functions of the gene.
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http://dx.doi.org/10.1186/1471-2148-11-98DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3101173PMC
April 2011