Publications by authors named "Mark Kirkpatrick"

84 Publications

Heterogeneous histories of recombination suppression on stickleback sex chromosomes.

Mol Biol Evol 2021 Jun 12. Epub 2021 Jun 12.

Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712.

How consistent are the evolutionary trajectories of sex chromosomes shortly after they form? Insights into the evolution of recombination, differentiation, and degeneration can be provided by comparing closely related species with homologous sex chromosomes. The sex chromosomes of the threespine stickleback (Gasterosteus aculeatus) and its sister species, the Japan Sea stickleback (G. nipponicus), have been well characterized. Little is known, however, about the sex chromosomes of their congener, the blackspotted stickleback (G. wheatlandi). We used pedigrees to obtain experimentally phased whole genome sequences from blackspotted stickleback X and Y chromosomes. Using multispecies gene trees and analysis of shared duplications, we demonstrate that Chromosome 19 is the ancestral sex chromosome and that its oldest stratum evolved in the common ancestor of the genus. After the blackspotted lineage diverged, its sex chromosomes experienced independent and more extensive recombination suppression, greater X-Y differentiation, and a much higher rate of Y degeneration than the other two species. These patterns may result from a smaller effective population size in the blackspotted stickleback. A recent fusion between the ancestral blackspotted stickleback Y chromosome and Chromosome 12, which produced a neo-X and neo-Y, may have been favored by the very small size of the recombining region on the ancestral sex chromosome. We identify six strata on the ancestral and neo-sex chromosomes where recombination between the X and Y ceased at different times. These results confirm that sex chromosomes can evolve large differences within and between species over short evolutionary timescales.
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http://dx.doi.org/10.1093/molbev/msab179DOI Listing
June 2021

Molecular evolution and the decline of purifying selection with age.

Nat Commun 2021 05 11;12(1):2657. Epub 2021 May 11.

Department of Integrative Biology, University of Texas, Austin, TX, USA.

Life history theory predicts that the intensity of selection declines with age, and this trend should impact how genes expressed at different ages evolve. Here we find consistent relationships between a gene's age of expression and patterns of molecular evolution in two mammals (the human Homo sapiens and the mouse Mus musculus) and two insects (the malaria mosquito Anopheles gambiae and the fruit fly Drosophila melanogaster). When expressed later in life, genes fix nonsynonymous mutations more frequently, are more polymorphic for nonsynonymous mutations, and have shorter evolutionary lifespans, relative to those expressed early. The latter pattern is explained by a simple evolutionary model. Further, early-expressed genes tend to be enriched in similar gene ontology terms across species, while late-expressed genes show no such consistency. In humans, late-expressed genes are more likely to be linked to cancer and to segregate for dominant disease-causing mutations. Last, the effective strength of selection (N s) decreases and the fraction of beneficial mutations increases with a gene's age of expression. These results are consistent with the diminishing efficacy of purifying selection with age, as proposed by Medawar's classic hypothesis for the evolution of senescence, and provide links between life history theory and molecular evolution.
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http://dx.doi.org/10.1038/s41467-021-22981-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8113359PMC
May 2021

Effect of serum total protein concentration on early-life health and growth of dairy calves.

J Am Vet Med Assoc 2020 Jul;257(1):80-86

Objective: To assess the effect of serum total protein (STP) concentration on the early-life health and growth of dairy calves.

Animals: 39,619 neonatal Holstein, Jersey, and crossbred calves from 15 dairy operations.

Procedures: Calves arrived at a single calf-raising facility at approximately 2 days old. Each calf was weighed at facility arrival, and a blood sample was obtained the next day for determination of STP concentration by refractometry. All calves were managed in a standard manner, and health events were recorded for 120 days. A subset of 3,214 calves was weighed at 120 days old, and the average daily gain (ADG) was calculated. Linear mixed models were used to assess the effect of STP concentration on specific health events.

Results: STP concentration was associated with the incidences of death, diarrhea, pneumonia, and whether a calf received IV fluid therapy. In general, the incidence of adverse health events decreased as STP concentration increased to 6.0 g/dL, plateaued at STP concentrations between 6.0 and 8.5 g/dL, and increased at STP concentrations > 8.5 g/dL. Although STP concentration was not associated with ADG, the ADG for Holsteins increased as STP concentration increased to 8.5 g/dL and then decreased at STP concentrations > 8.5 g/dL.

Conclusions And Clinical Relevance: Results suggested that, for neonatal dairy calves, an STP concentration between 6.0 and 8.5 g/dL was optimal for health and growth, and calves with an STP concentration < 5.0 or > 8.5 g/dL should be considered at high risk for adverse health events.
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http://dx.doi.org/10.2460/javma.257.1.80DOI Listing
July 2020

The signal of sex-specific selection in humans is not an artefact: Reply to Mank et al.

Mol Ecol 2020 04 27;29(8):1406-1407. Epub 2020 Apr 27.

Department of Integrative Biology, University of Texas, Austin, TX, USA.

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http://dx.doi.org/10.1111/mec.15420DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7537717PMC
April 2020

Sex Differences in the Recombination Landscape.

Am Nat 2020 02 9;195(2):361-379. Epub 2019 Dec 9.

Sex differences in overall recombination rates are well known, but little theoretical or empirical attention has been given to how and why sexes differ in their recombination landscapes: the patterns of recombination along chromosomes. In the first scientific review of this phenomenon, we find that recombination is biased toward telomeres in males and more uniformly distributed in females in most vertebrates and many other eukaryotes. Notable exceptions to this pattern exist, however. Fine-scale recombination patterns also frequently differ between males and females. The molecular mechanisms responsible for sex differences remain unclear, but chromatin landscapes play a role. Why these sex differences evolve also is unclear. Hypotheses suggest that they may result from sexually antagonistic selection acting on coding genes and their regulatory elements, meiotic drive in females, selection during the haploid phase of the life cycle, selection against aneuploidy, or mechanistic constraints. No single hypothesis, however, can adequately explain the evolution of sex differences in all cases. Sex-specific recombination landscapes have important consequences for population differentiation and sex chromosome evolution.
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http://dx.doi.org/10.1086/704943DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7537610PMC
February 2020

The evolution of hybrid fitness during speciation.

PLoS Genet 2019 05 6;15(5):e1008125. Epub 2019 May 6.

Integrative Biology Department, University of Texas at Austin, Austin, Texas, United States of America.

The evolution of postzygotic reproductive isolation is an important component of speciation. But before isolation is complete there is sometimes a phase of heterosis in which hybrid fitness exceeds that of the two parental species. The genetics and evolution of heterosis and postzygotic isolation have typically been studied in isolation, precluding the development of a unified theory of speciation. Here, we develop a model that incorporates both positive and negative gene interactions, and accounts for the evolution of both heterosis and postzygotic isolation. We parameterize the model with recent data on the fitness effects of 10,000 mutations in yeast, singly and in pairwise epistatic combinations. The model makes novel predictions about the types of interactions that contribute to declining hybrid fitness. We reproduce patterns familiar from earlier models of speciation (e.g. Haldane's Rule and Darwin's Corollary) and identify new mechanisms that may underlie these patterns. Our approach provides a general framework for integrating experimental data from gene interaction networks into speciation theory and makes new predictions about the genetic mechanisms of speciation.
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http://dx.doi.org/10.1371/journal.pgen.1008125DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6502311PMC
May 2019

A reciprocal translocation radically reshapes sex-linked inheritance in the common frog.

Mol Ecol 2019 04 29;28(8):1877-1889. Epub 2019 Apr 29.

Department of Integrative Biology, University of Texas, Austin, Texas.

X and Y chromosomes can diverge when rearrangements block recombination between them. Here we present the first genomic view of a reciprocal translocation that causes two physically unconnected pairs of chromosomes to be coinherited as sex chromosomes. In a population of the common frog (Rana temporaria), both pairs of X and Y chromosomes show extensive sequence differentiation, but not degeneration of the Y chromosomes. A new method based on gene trees shows both chromosomes are sex-linked. Furthermore, the gene trees from the two Y chromosomes have identical topologies, showing they have been coinherited since the reciprocal translocation occurred. Reciprocal translocations can thus reshape sex linkage on a much greater scale compared with inversions, the type of rearrangement that is much better known in sex chromosome evolution, and they can greatly amplify the power of sexually antagonistic selection to drive genomic rearrangement. Two more populations show evidence of other rearrangements, suggesting that this species has unprecedented structural polymorphism in its sex chromosomes.
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http://dx.doi.org/10.1111/mec.14990DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7558804PMC
April 2019

The Origin of a New Sex Chromosome by Introgression between Two Stickleback Fishes.

Mol Biol Evol 2019 01;36(1):28-38

Department of Integrative Biology, University of Texas, Austin, TX.

Introgression is increasingly recognized as a source of genetic diversity that fuels adaptation. Its role in the evolution of sex chromosomes, however, is not well known. Here, we confirm the hypothesis that the Y chromosome in the ninespine stickleback, Pungitius pungitius, was established by introgression from the Amur stickleback, P. sinensis. Using whole genome resequencing, we identified a large region of Chr 12 in P. pungitius that is diverged between males and females. Within but not outside of this region, several lines of evidence show that the Y chromosome of P. pungitius shares a most recent common ancestor not with the X chromosome, but with the homologous chromosome in P. sinensis. Accumulation of repetitive elements and gene expression changes on the new Y are consistent with a young sex chromosome in early stages of degeneration, but other hallmarks of Y chromosomes have not yet appeared. Our findings indicate that porous species boundaries can trigger rapid sex chromosome evolution.
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http://dx.doi.org/10.1093/molbev/msy181DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6340465PMC
January 2019

Inversions are bigger on the X chromosome.

Mol Ecol 2019 03 29;28(6):1238-1245. Epub 2018 Aug 29.

Department of Integrative Biology, University of Texas, Austin, Texas.

In many insects, X-linked inversions fix at a higher rate and are much less polymorphic than autosomal inversions. Here, we report that in Drosophila, X-linked inversions also capture 67% more genes. We estimated the number of genes captured through an approximate Bayesian computational analysis of gene orders in nine species of Drosophila. X-linked inversions fixed with a significantly larger gene content. Further, X-linked inversions of intermediate size enjoy highest fixation rate, while the fixation rate of autosomal inversions decreases with size. A less detailed analysis in Anopheles suggests a similar pattern holds in mosquitoes. We develop a population genetic model that assumes the fitness effects of inversions scale with the number of genes captured. We show that the same conditions that lead to a higher fixation rate also produce a larger size for inversions on the X.
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http://dx.doi.org/10.1111/mec.14819DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6353710PMC
March 2019

Sex Differences in Recombination in Sticklebacks.

G3 (Bethesda) 2018 05 31;8(6):1971-1983. Epub 2018 May 31.

Department of Integrative Biology, University of Texas at Austin, Texas 78712.

Recombination often differs markedly between males and females. Here we present the first analysis of sex-specific recombination in sticklebacks. Using whole-genome sequencing of 15 crosses between and , we localized 698 crossovers with a median resolution of 2.3 kb. We also used a bioinformatic approach to infer historical sex-averaged recombination patterns for both species. Recombination is greater in females than males on all chromosomes, and overall map length is 1.64 times longer in females. The locations of crossovers differ strikingly between sexes. Crossovers cluster toward chromosome ends in males, but are distributed more evenly across chromosomes in females. Suppression of recombination near the centromeres in males causes crossovers to cluster at the ends of long arms in acrocentric chromosomes, and greatly reduces crossing over on short arms. The effect of centromeres on recombination is much weaker in females. Genomic differentiation between and is strongly correlated with recombination rate, and patterns of differentiation along chromosomes are strongly influenced by male-specific telomere and centromere effects. We found no evidence for fine-scale correlations between recombination and local gene content in either sex. We discuss hypotheses for the origin of sexual dimorphism in recombination and its consequences for sexually antagonistic selection and sex chromosome evolution.
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http://dx.doi.org/10.1534/g3.118.200166DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5982825PMC
May 2018

Environmental Plasticity in the Intersexual Correlation and Sex Bias of Gene Expression.

J Hered 2017 10;108(7):754-758

Department of Integrative Biology, University of Texas, Austin, TX 78712.

Intersexual genetic correlations are expected to constrain the evolution of sexual dimorphic traits, including the degree of sex-biased gene expression. Consistent with that expectation, studies in fruit flies and birds have reported that genes whose expression has a strong intersexual genetic correlation (rMF) show a lower level of sex-biased expression (SBE). However, it is known that both rMF and SBE can be affected by the environment. It is therefore unclear whether there is a consistent relationship between these 2 quantities across multiple environments. In this paper, we study this relationship in the African malaria mosquito Anopheles gambiae. We show that both rMF and SBE change between environments. The change in SBE across environments is significantly correlated with dN/dS: greater changes in SBE are associated with higher values of dN/dS. Furthermore, the relationship between rMF and SBE is sensitive to the environment. We conclude that this relationship is sufficiently plastic that environmental effects should be considered in future studies.
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http://dx.doi.org/10.1093/jhered/esx083DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6281341PMC
October 2017

Extensive Genetic Differentiation between Homomorphic Sex Chromosomes in the Mosquito Vector, Aedes aegypti.

Genome Biol Evol 2017 09;9(9):2322-2335

Department of Genomes and Genetics, Insect-Virus Interactions Group, Institut Pasteur, Paris, France.

Mechanisms and evolutionary dynamics of sex-determination systems are of particular interest in insect vectors of human pathogens like mosquitoes because novel control strategies aim to convert pathogen-transmitting females into nonbiting males, or rely on accurate sexing for the release of sterile males. In Aedes aegypti, the main vector of dengue and Zika viruses, sex determination is governed by a dominant male-determining locus, previously thought to reside within a small, nonrecombining, sex-determining region (SDR) of an otherwise homomorphic sex chromosome. Here, we provide evidence that sex chromosomes in Ae. aegypti are genetically differentiated between males and females over a region much larger than the SDR. Our linkage mapping intercrosses failed to detect recombination between X and Y chromosomes over a 123-Mbp region (40% of their physical length) containing the SDR. This region of reduced male recombination overlapped with a smaller 63-Mbp region (20% of the physical length of the sex chromosomes) displaying high male-female genetic differentiation in unrelated wild populations from Brazil and Australia and in a reference laboratory strain originating from Africa. In addition, the sex-differentiated genomic region was associated with a significant excess of male-to-female heterozygosity and contained a small cluster of loci consistent with Y-specific null alleles. We demonstrate that genetic differentiation between sex chromosomes is sufficient to assign individuals to their correct sex with high accuracy. We also show how data on allele frequency differences between sexes can be used to estimate linkage disequilibrium between loci and the sex-determining locus. Our discovery of large-scale genetic differentiation between sex chromosomes in Ae. aegypti lays a new foundation for mapping and population genomic studies, as well as for mosquito control strategies targeting the sex-determination pathway.
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http://dx.doi.org/10.1093/gbe/evx171DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5737474PMC
September 2017

Chromosomal Speciation in the Genomics Era: Disentangling Phylogenetic Evolution of Rock-wallabies.

Front Genet 2017 10;8:10. Epub 2017 Feb 10.

Research School of Biology, Australian National University, Acton ACT, Australia.

The association of chromosome rearrangements (CRs) with speciation is well established, and there is a long history of theory and evidence relating to "chromosomal speciation." Genomic sequencing has the potential to provide new insights into how reorganization of genome structure promotes divergence, and in model systems has demonstrated reduced gene flow in rearranged segments. However, there are limits to what we can understand from a small number of model systems, which each only tell us about one episode of chromosomal speciation. Progressing from patterns of association between chromosome (and genic) change, to understanding processes of speciation requires both comparative studies across diverse systems and integration of genome-scale sequence comparisons with other lines of evidence. Here, we showcase a promising example of chromosomal speciation in a non-model organism, the endemic Australian marsupial genus . We present initial phylogenetic results from exon-capture that resolve a history of divergence associated with extensive and repeated CRs. Yet it remains challenging to disentangle gene tree heterogeneity caused by recent divergence and gene flow in this and other such recent radiations. We outline a way forward for better integration of comparative genomic sequence data with evidence from molecular cytogenetics, and analyses of shifts in the recombination landscape and potential disruption of meiotic segregation and epigenetic programming. In all likelihood, CRs impact multiple cellular processes and these effects need to be considered together, along with effects of genic divergence. Understanding the effects of CRs together with genic divergence will require development of more integrative theory and inference methods. Together, new data and analysis tools will combine to shed light on long standing questions of how chromosome and genic divergence promote speciation.
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http://dx.doi.org/10.3389/fgene.2017.00010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5301020PMC
February 2017

Sex-Specific Selection and Sex-Biased Gene Expression in Humans and Flies.

PLoS Genet 2016 Sep 22;12(9):e1006170. Epub 2016 Sep 22.

Department of Integrative Biology, University of Texas, Austin, Texas, United States of America.

Sexual dimorphism results from sex-biased gene expression, which evolves when selection acts differently on males and females. While there is an intimate connection between sex-biased gene expression and sex-specific selection, few empirical studies have studied this relationship directly. Here we compare the two on a genome-wide scale in humans and flies. We find a distinctive "Twin Peaks" pattern in humans that relates the strength of sex-specific selection, quantified by genetic divergence between male and female adults at autosomal loci, to the degree of sex-biased expression. Genes with intermediate degrees of sex-biased expression show evidence of ongoing sex-specific selection, while genes with either little or completely sex-biased expression do not. This pattern apparently results from differential viability selection in males and females acting in the current generation. The Twin Peaks pattern is also found in Drosophila using a different measure of sex-specific selection acting on fertility. We develop a simple model that successfully recapitulates the Twin Peaks. Our results suggest that many genes with intermediate sex-biased expression experience ongoing sex-specific selection in humans and flies.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5033347PMC
http://dx.doi.org/10.1371/journal.pgen.1006170DOI Listing
September 2016

The Evolution of Genome Structure by Natural and Sexual Selection.

Authors:
Mark Kirkpatrick

J Hered 2017 01 7;108(1):3-11. Epub 2016 Jul 7.

From the Department of Integrative Biology C-0990, University of Texas, Austin, TX 78712 USA (Kirkpatrick).

Progress on understanding how genome structure evolves is accelerating with the arrival of new genomic, comparative, and theoretical approaches. This article reviews progress in understanding how chromosome inversions and sex chromosomes evolve, and how their evolution affects species' ecology. Analyses of clines in inversion frequencies in flies and mosquitoes imply strong local adaptation, and roles for both over- and under dominant selection. Those results are consistent with the hypothesis that inversions become established when they capture locally adapted alleles. Inversions can carry alleles that are beneficial to closely related species, causing them to introgress following hybridization. Models show that this "adaptive cassette" scenario can trigger large range expansions, as recently happened in malaria mosquitoes. Sex chromosomes are the most rapidly evolving genome regions of some taxa. Sexually antagonistic selection may be the key force driving transitions of sex determination between different pairs of chromosomes and between XY and ZW systems. Fusions between sex-chromosomes and autosomes most often involve the Y chromosome, a pattern that can be explained if fusions are mildly deleterious and fix by drift. Sexually antagonistic selection is one of several hypotheses to explain the recent discovery that the sex determination system has strong effects on the adult sex ratios of tetrapods. The emerging view of how genome structure evolves invokes a much richer constellation of forces than was envisioned during the Golden Age of research on Drosophila karyotypes.
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http://dx.doi.org/10.1093/jhered/esw041DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5155700PMC
January 2017

Prezygotic isolation, mating preferences, and the evolution of chromosomal inversions.

Evolution 2016 07 30;70(7):1465-72. Epub 2016 May 30.

Department of Integrative Biology, University of Texas, Austin, Texas, 78712.

Chromosomal inversions are frequently implicated in isolating species. Models have shown how inversions can evolve in the context of postmating isolation. Inversions are also frequently associated with mating preferences, a topic that has not been studied theoretically. Here, we show how inversions can spread by capturing a mating preference locus and one or more loci involved with epistatic incompatibilities. Inversions can be established under broad conditions ranging from near panmixis to nearly complete speciation. These results provide a hypothesis to explain the growing number of examples of inversions associated with premating isolating mechanisms.
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http://dx.doi.org/10.1111/evo.12954DOI Listing
July 2016

Compensatory Drift and the Evolutionary Dynamics of Dosage-Sensitive Duplicate Genes.

Genetics 2016 Feb 12;202(2):765-74. Epub 2015 Dec 12.

Department of Integrative Biology, University of Texas, Austin, Texas 78712.

Dosage-balance selection preserves functionally redundant duplicates (paralogs) at the optimum for their combined expression. Here we present a model of the dynamics of duplicate genes coevolving under dosage-balance selection. We call this the compensatory drift model. Results show that even when strong dosage-balance selection constrains total expression to the optimum, expression of each duplicate can diverge by drift from its original level. The rate of divergence slows as the strength of stabilizing selection, the size of the mutation effect, and/or the size of the population increases. We show that dosage-balance selection impedes neofunctionalization early after duplication but can later facilitate it. We fit this model to data from sodium channel duplicates in 10 families of teleost fish; these include two convergent lineages of electric fish in which one of the duplicates neofunctionalized. Using the model, we estimated the strength of dosage-balance selection for these genes. The results indicate that functionally redundant paralogs still may undergo radical functional changes after a prolonged period of compensatory drift.
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http://dx.doi.org/10.1534/genetics.115.178137DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4788248PMC
February 2016

The genetic sex-determination system predicts adult sex ratios in tetrapods.

Nature 2015 Nov 7;527(7576):91-4. Epub 2015 Oct 7.

Department of Limnology, University of Pannonia, Pf. 158, H-8201 Veszprém, Hungary.

The adult sex ratio (ASR) has critical effects on behaviour, ecology and population dynamics, but the causes of variation in ASRs are unclear. Here we assess whether the type of genetic sex determination influences the ASR using data from 344 species in 117 families of tetrapods. We show that taxa with female heterogamety have a significantly more male-biased ASR (proportion of males: 0.55 ± 0.01 (mean ± s.e.m.)) than taxa with male heterogamety (0.43 ± 0.01). The genetic sex-determination system explains 24% of interspecific variation in ASRs in amphibians and 36% in reptiles. We consider several genetic factors that could contribute to this pattern, including meiotic drive and sex-linked deleterious mutations, but further work is needed to quantify their effects. Regardless of the mechanism, the effects of the genetic sex-determination system on the adult sex ratio are likely to have profound effects on the demography and social behaviour of tetrapods.
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http://dx.doi.org/10.1038/nature15380DOI Listing
November 2015

Y fuse? Sex chromosome fusions in fishes and reptiles.

PLoS Genet 2015 May 20;11(5):e1005237. Epub 2015 May 20.

Ecological Genetics Laboratory, National Institute of Genetics, Mishima, Shizuoka, Japan.

Chromosomal fusion plays a recurring role in the evolution of adaptations and reproductive isolation among species, yet little is known of the evolutionary drivers of chromosomal fusions. Because sex chromosomes (X and Y in male heterogametic systems, Z and W in female heterogametic systems) differ in their selective, mutational, and demographic environments, those differences provide a unique opportunity to dissect the evolutionary forces that drive chromosomal fusions. We estimate the rate at which fusions between sex chromosomes and autosomes become established across the phylogenies of both fishes and squamate reptiles. Both the incidence among extant species and the establishment rate of Y-autosome fusions is much higher than for X-autosome, Z-autosome, or W-autosome fusions. Using population genetic models, we show that this pattern cannot be reconciled with many standard explanations for the spread of fusions. In particular, direct selection acting on fusions or sexually antagonistic selection cannot, on their own, account for the predominance of Y-autosome fusions. The most plausible explanation for the observed data seems to be (a) that fusions are slightly deleterious, and (b) that the mutation rate is male-biased or the reproductive sex ratio is female-biased. We identify other combinations of evolutionary forces that might in principle account for the data although they appear less likely. Our results shed light on the processes that drive structural changes throughout the genome.
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http://dx.doi.org/10.1371/journal.pgen.1005237DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4439076PMC
May 2015

Expansion load and the evolutionary dynamics of a species range.

Am Nat 2015 Apr;185(4):E81-93

Institute of Ecology and Evolution, University of Berne, 3012 Berne, Switzerland; and Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland.

Expanding populations incur a mutation burden, the so-called expansion load. Using a mixture of individual-based simulations and analytical modeling, we study the expansion load process in models where population growth depends on the population's fitness (i.e., hard selection). We show that expansion load can severely slow down expansions and limit a species' range, even in the absence of environmental variation. We also study the effect of recombination on the dynamics of a species range and on the evolution of mean fitness on the wave front. If recombination is strong, mean fitness on front approaches an equilibrium value at which the effects of fixed mutations cancel each other out. The equilibrium rate at which new demes are colonized is similar to the rate at which beneficial mutations spread through the core. Without recombination, the dynamics is more complex, and beneficial mutations from the core of the range can invade the front of the expansion, which results in irregular and episodic expansion. Although the rate of adaptation is generally higher in recombining organisms, the mean fitness on the front may be larger in the absence of recombination because high-fitness individuals from the core have a higher chance to invade the front. Our findings have important consequences for the evolutionary dynamics of species ranges as well as on the role and the evolution of recombination during range expansions.
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http://dx.doi.org/10.1086/680220DOI Listing
April 2015

Chromosome inversions, adaptive cassettes and the evolution of species' ranges.

Mol Ecol 2015 May 6;24(9):2046-55. Epub 2015 Feb 6.

Department of Integrative Biology, University of Texas, Austin, TX, 78712, USA.

A chromosome inversion can spread when it captures locally adapted alleles or when it is introduced into a species by hybridization with adapted alleles that were previously absent. We present a model that shows how both processes can cause a species range to expand. Introgression of an inversion that carries novel, locally adapted alleles is a particularly powerful mechanism for range expansion. The model supports the earlier proposal that introgression of an inversion triggered a large range expansion of a malaria mosquito. These results suggest a role for inversions as cassettes of genes that can accelerate adaptation by crossing species boundaries, rather than protecting genomes from introgression.
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http://dx.doi.org/10.1111/mec.13074DOI Listing
May 2015

Ontogenetic stage-specific quantitative trait loci contribute to divergence in developmental trajectories of sexually dimorphic fins between medaka populations.

Mol Ecol 2014 Nov 13;23(21):5258-75. Epub 2014 Oct 13.

Ecological Genetics Laboratory, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, 411-8540, Japan.

Sexual dimorphism can evolve when males and females differ in phenotypic optima. Genetic constraints can, however, limit the evolution of sexual dimorphism. One possible constraint is derived from alleles expressed in both sexes. Because males and females share most of their genome, shared alleles with different fitness effects between sexes are faced with intralocus sexual conflict. Another potential constraint is derived from genetic correlations between developmental stages. Sexually dimorphic traits are often favoured at adult stages, but selected against as juvenile, so developmental decoupling of traits between ontogenetic stages may be necessary for the evolution of sexual dimorphism in adults. Resolving intralocus conflicts between sexes and ages is therefore a key to the evolution of age-specific expression of sexual dimorphism. We investigated the genetic architecture of divergence in the ontogeny of sexual dimorphism between two populations of the Japanese medaka (Oryzias latipes) that differ in the magnitude of dimorphism in anal and dorsal fin length. Quantitative trait loci (QTL) mapping revealed that few QTL had consistent effects throughout ontogenetic stages and the majority of QTL change the sizes and directions of effects on fin growth rates during ontogeny. We also found that most QTL were sex-specific, suggesting that intralocus sexual conflict is almost resolved. Our results indicate that sex- and age-specific QTL enable the populations to achieve optimal developmental trajectories of sexually dimorphic traits in response to complex natural and sexual selection.
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http://dx.doi.org/10.1111/mec.12933DOI Listing
November 2014

Strong reinforcing selection in a Texas wildflower.

Curr Biol 2014 Sep 21;24(17):1995-9. Epub 2014 Aug 21.

Department of Integrative Biology, The University of Texas at Austin, Austin, TX 78712, USA.

Reinforcement, the process of increased reproductive isolation due to selection against hybrids, is an important mechanism by which natural selection contributes to speciation [1]. Empirical studies suggest that reinforcement has generated reproductive isolation in many taxa (reviewed in [2-4]), and theoretical work shows it can act under broad selective conditions [5-11]. However, the strength of selection driving reinforcement has never been measured in nature. Here, we quantify the strength of reinforcing selection in the Texas wildflower Phlox drummondii using a strategy that weds a population genetic model with field data. Reinforcement in this system is caused by variation in two loci that affect flower color [12]. We quantify sharp clines in flower color where this species comes into contact with its congener, Phlox cuspidata. We develop a spatially explicit population genetic model for these clines based on the known genetics of flower color. We fit our model to the data using likelihood, and we searched parameter space using Markov chain Monte Carlo methods. We find that selection on flower color genes generated by reinforcement is exceptionally strong. Our findings demonstrate that natural selection can play a decisive role in the evolution of reproductive isolation through the process of reinforcement.
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http://dx.doi.org/10.1016/j.cub.2014.07.027DOI Listing
September 2014

Matrix inversions for chromosomal inversions: a method to construct summary statistics in complex coalescent models.

Theor Popul Biol 2014 Nov 1;97:1-10. Epub 2014 Aug 1.

Section of Integrative Biology, University of Texas, Austin, TX 78712, USA. Electronic address:

Chromosomal inversions allow genetic divergence of locally adapted populations by reducing recombination between chromosomes with different arrangements. While patterns of genetic variation within inverted regions are increasingly documented, inferential methods are largely missing to analyze such data. Previous work has provided expectations for coalescence patterns of neutral sites linked to an inversion polymorphism in two locally adapted populations. Here, we define a method to construct summary statistics in such complex population structure models. Under a scenario of selection on the inversion breakpoints, we first construct estimators of the migration rate between the two habitats, and of the recombination rate of a nucleotide site between the two inversion backgrounds. Next, we analyze the disequilibrium between two sites within an inversion and provide an estimator of the distinct recombination rate between these two sites in homokaryotypes and heterokaryotypes. These estimators should be suitable summary statistics for simulation-based methods that can handle the complex dependences in the data.
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http://dx.doi.org/10.1016/j.tpb.2014.07.005DOI Listing
November 2014

Sex determination: why so many ways of doing it?

PLoS Biol 2014 Jul 1;12(7):e1001899. Epub 2014 Jul 1.

University of Calgary, Department of Biological Sciences, Calgary, Alberta, Canada.

Sexual reproduction is an ancient feature of life on earth, and the familiar X and Y chromosomes in humans and other model species have led to the impression that sex determination mechanisms are old and conserved. In fact, males and females are determined by diverse mechanisms that evolve rapidly in many taxa. Yet this diversity in primary sex-determining signals is coupled with conserved molecular pathways that trigger male or female development. Conflicting selection on different parts of the genome and on the two sexes may drive many of these transitions, but few systems with rapid turnover of sex determination mechanisms have been rigorously studied. Here we survey our current understanding of how and why sex determination evolves in animals and plants and identify important gaps in our knowledge that present exciting research opportunities to characterize the evolutionary forces and molecular pathways underlying the evolution of sex determination.
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http://dx.doi.org/10.1371/journal.pbio.1001899DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4077654PMC
July 2014

Local adaptation and the evolution of chromosome fusions.

Evolution 2014 Oct 1;68(10):2747-56. Epub 2014 Aug 1.

Department of Integrative Biology C-0990, University of Texas, Austin, Texas, 78712.

We use forward and coalescent models of population genetics to study chromosome fusions that reduce the recombination between two locally adapted loci. Under a continent-island model, a fusion spreads and reaches a polymorphic equilibrium when it causes recombination between locally adapted alleles to be less than their selective advantage. In contrast, fusions in a two-deme model always spread; whether it reaches a polymorphic equilibrium or becomes fixed depends on the relative recombination rates of fused homozygotes and heterozygotes. Neutral divergence around fusion polymorphisms is markedly increased, showing peaks at the point of fusion and at the locally adapted loci. Local adaptation could explain the evolution of many of chromosome fusions, which are some of the most common chromosome rearrangements in nature.
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http://dx.doi.org/10.1111/evo.12481DOI Listing
October 2014

Signatures of sex-antagonistic selection on recombining sex chromosomes.

Genetics 2014 Jun 27;197(2):531-41. Epub 2014 Feb 27.

Department of Integrative Biology, University of Texas, Austin, Texas 78712.

Sex-antagonistic (SA) selection has major evolutionary consequences: it can drive genomic change, constrain adaptation, and maintain genetic variation for fitness. The recombining (or pseudoautosomal) regions of sex chromosomes are a promising setting in which to study SA selection because they tend to accumulate SA polymorphisms and because recombination allows us to deploy the tools of molecular evolution to locate targets of SA selection and quantify evolutionary forces. Here we use coalescent models to characterize the patterns of polymorphism expected within and divergence between recombining X and Y (or Z and W) sex chromosomes. SA selection generates peaks of divergence between X and Y that can extend substantial distances away from the targets of selection. Linkage disequilibrium between neutral sites is also inflated. We show how the pattern of divergence is altered when the SA polymorphism or the sex-determining region was recently established. We use data from the flowering plant Silene latifolia to illustrate how the strength of SA selection might be quantified using molecular data from recombining sex chromosomes.
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http://dx.doi.org/10.1534/genetics.113.156026DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4063913PMC
June 2014

Long range linkage disequilibrium across the human genome.

PLoS One 2013 12;8(12):e80754. Epub 2013 Dec 12.

Department of Integrative Biology, University of Texas, Austin, Texas, United States of America.

Long-range linkage disequilibria (LRLD) between sites that are widely separated on chromosomes may suggest that population admixture, epistatic selection, or other evolutionary forces are at work. We quantified patterns of LRLD on a chromosome-wide level in the YRI population of the HapMap dataset of single nucleotide polymorphisms (SNPs). We calculated the disequilibrium between all pairs of SNPs on each chromosome (a total of >2×10(11) values) and evaluated significance of overall disequilibrium using randomization. The results show an excess of associations between pairs of distant sites (separated by >0.25 cM) on all of the 22 autosomes. We discuss possible explanations for this observation.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0080754PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3861250PMC
September 2014

Evolution of a genetic incompatibility in the genus Xiphophorus.

Mol Biol Evol 2013 Oct 27;30(10):2302-10. Epub 2013 Jul 27.

Section of Integrative Biology, University of Texas, Austin.

Genetic incompatibilities are commonly observed between hybridizing species. Although this type of isolating mechanism has received considerable attention, we have few examples describing how genetic incompatibilities evolve. We investigated the evolution of two loci involved in a classic example of a Bateson-Dobzhansky-Muller (BDM) incompatibility in Xiphophorus, a genus of freshwater fishes from northern Central America. Hybrids develop a lethal melanoma due to the interaction of two loci, an oncogene and its repressor. We cloned and sequenced the putative repressor locus in 25 Xiphophorus species and an outgroup species, and determined the status of the oncogene in those species from the literature. Using phylogenetic analyses, we find evidence that a repeat region in the proximal promoter of the repressor is coevolving with the oncogene. The data support a hypothesis that departs from the standard BDM model: it appears the alleles that cause the incompatibilities have coevolved simultaneously within lineages, rather than in allopatric or temporal isolation.
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http://dx.doi.org/10.1093/molbev/mst127DOI Listing
October 2013