Find research datasets worth reusing

Data from: A new approach to chromosomal evolution in the giant water bug (Heteroptera: Belostomatidae)

The genus Belostoma, known colloquially as 'giant water bugs', presents striking cytogenetic diversity and extensive chromosome variability. Notwithstanding, its karyotype evolution is not well understood. We analyzed eight species of Belostoma (77 samples). The meiotic analysis revealed 2n=14+XY for B. horvathi and B. candidulum; 2n=22+XY for B. cummings; 2n=26+X1X2Y for B. dentatum, B. elongatum, and B. discretum; and 2n=26+X1X2X3Y for B. testacopallidum and B. dilatatum. All species showed holokinetic chromosomes. Based on heterochromatin distribution patterns and 18S rDNA, the species of the genus Belostoma were separated into four groups. The analysis of C0t-1 DNA showed that the repetitive DNA, partly composed of microsatellite DNA, was absent on the Y chromosome. FISH using a microdissected X chromosome in species with simple sex system presents uniform hybridization in the nuclear region corresponding to the X chromosome. Species with multiple systems revealed discrete markings. The present data in conjunction with the existing literature led us to propose a new evolutionary hypothesis for the group, with an ancestral karyotype with a low diploid number, simple sex determination system, and Nucleolus Organizer Regions (NORs) on the sex chromosomes. That karyotype would have originated other karyotypes through agmatoploidy, simploidy, heterochromatinization, and movement of the 18S rDNA.

Data from: Chromosomal speciation in the genomics era: disentangling phylogenetic evolution of rock-wallabies

The association of chromosome rearrangements 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 Petrogale. We present initial phylogenetic results from exon-capture that resolve a history of divergence associated with extensive and repeated chromosome rearrangements. 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, chromosome rearrangements impact multiple cellular processes and these effects need to be considered together, along with those of genic divergence. Understanding the effects of chromosome rearrangements 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.

Data from: The last bastion? X chromosome genotyping of Anopheles gambiae species pair males from a hybrid zone reveals complex recombination within the major candidate 'genomic island of speciation'

Speciation with gene flow may be aided by reduced recombination helping to build linkage between genes involved in the early stages of reproductive isolation. Reduced recombination on chromosome X has been implicated in speciation within the Anopheles gambiae complex, species of which represent the major Afrotropical malaria vectors. The most recently diverged, morphologically indistinguishable, species pair, A. gambiae and Anopheles coluzzii, ubiquitously displays a 'genomic island of divergence' spanning over 4 Mb from chromosome X centromere, which represents a particularly promising candidate region for reproductive isolation genes, in addition to containing the diagnostic markers used to distinguish the species. Very low recombination makes the island intractable for experimental recombination studies, but an extreme hybrid zone in Guinea Bissau offers the opportunity for natural investigation of X-island recombination. SNP analysis of chromosome X hemizygous males revealed: (i) strong divergence in the X-island despite a lack of autosomal divergence; (ii) individuals with multiple-recombinant genotypes, including likely double crossovers and localized gene conversion; (iii) recombination-driven discontinuity both within and between the molecular species markers, suggesting that the utility of the diagnostics is undermined under high hybridization. The largely, but incompletely protected nature of the X centromeric genomic island is consistent with a primary candidate area for accumulation of adaptive variants driving speciation with gene flow, while permitting some selective shuffling and removal of genetic variation.

Data from: A rare exception to Haldane's rule: Are X chromosomes key to hybrid incompatibilities?

The prevalence of Haldane's rule suggests that sex chromosomes commonly have a key role in reproductive barriers and speciation. However, the majority of research on Haldane's rule has been conducted in species with conventional sex determination systems (XY and ZW) and exceptions to the rule have been understudied. Here we test the role of X-linked incompatibilities in a rare exception to Haldane's rule for female sterility in field cricket sister species (Teleogryllus oceanicus and T. commodus). Both have an XO sex determination system. Using three generations of crosses, we introgressed X chromosomes from each species onto different, mixed genomic backgrounds to test predictions about the fertility and viability of each cross type. We predicted that females with two different species X chromosomes would suffer reduced fertility and viability compared with females with two parental X chromosomes. However, we found no strong support for such X-linked incompatibilities. Our results preclude X–X incompatibilities and instead support an interchromosomal epistatic basis to hybrid female sterility. We discuss the broader implications of these findings, principally whether deviations from Haldane's rule might be more prevalent in species without dimorphic sex chromosomes.

Data from: The impact of reconstruction methods, phylogenetic uncertainty and branch lengths on inference of chromosome number evolution in American daisies (Melampodium, Asteraceae)

Chromosome number change (polyploidy and dysploidy) plays an important role in plant diversification and speciation. Investigating chromosome number evolution commonly entails ancestral state reconstruction performed within a phylogenetic framework, which is, however, prone to uncertainty, whose effects on evolutionary inferences are insufficiently understood. Using the chromosomally diverse plant genus Melampodium (Asteraceae) as model group, we assess the impact of reconstruction method (maximum parsimony, maximum likelihood, Bayesian methods), branch length model (phylograms versus chronograms) and phylogenetic uncertainty (topological and branch length uncertainty) on the inference of chromosome number evolution. We also address the suitability of the maximum clade credibility (MCC) tree as single representative topology for chromosome number reconstruction. Each of the listed factors causes considerable incongruence among chromosome number reconstructions. Discrepancies between inferences on the MCC tree from those made by integrating over a set of trees are moderate for ancestral chromosome numbers, but severe for the difference of chromosome gains and losses, a measure of the directionality of dysploidy. Therefore, reliance on single trees, such as the MCC tree, is strongly discouraged and model averaging, taking both phylogenetic and model uncertainty into account, is recommended. For studying chromosome number evolution, dedicated models implemented in the program ChromEvol and ordered maximum parsimony may be most appropriate. Chromosome number evolution in Melampodium follows a pattern of bidirectional dysploidy (starting from x = 11 to x = 9 and x = 14, respectively) with no prevailing direction.

opencc-zeroDec 2011View details →

Data from: Cryptic recombination in the ever-young sex chromosomes of Hylid frogs

Sex chromosomes are expected to evolve suppressed recombination, which leads to degeneration of the Y and heteromorphism between the X and Y. Some sex chromosomes remain homomorphic, however, and the factors that prevent degeneration of the Y in these cases are not understood. The homomorphic sex chromosomes of the European tree frogs (Hyla spp.) present an interesting paradox. Recombination in males has never been observed in crossing experiments, but molecular data are suggestive of occasional recombination between the X and Y. The hypothesis that these sex chromosomes recombine has not been tested statistically, however, nor has the XY recombination rate been estimated. Here we use Approximate Bayesian Computation coupled with coalescent simulations of sex chromosomes to quantify X-Y recombination rate from existent data. We find that microsatellite data from H. arborea, H. intermedia, and H. molleri support a recombination rate between X and Y that is significantly different from zero. We estimate that rate to be approximately 105 times smaller than that between X chromosomes. Our findings support the notion that very low recombination rate may be sufficient to maintain homomorphism in sex chromosomes.

opencc-zeroDec 2013View details →

Data from: Divergent population structure and climate associations of a chromosomal inversion polymorphism across the Mimulus guttatus species complex

Chromosomal rearrangement polymorphisms are common and increasingly found to be associated with adaptive ecological divergence and speciation. Rearrangements, such as inversions, reduce recombination in heterozygous individuals and thus can protect favorable allelic combinations at linked loci, facilitating their spread in the presence of gene flow. Recently, we identified a chromosomal inversion polymorphism that contributes to ecological adaptation and reproductive isolation between annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus. Here we evaluate the population genetic structure of this inverted region in comparison with the collinear regions of the genome across the M. guttatus species complex. We tested whether annual and perennial M. guttatus exhibit different patterns of divergence for loci in the inverted and noninverted regions of the genome. We then evaluated whether there are contrasting climate associations with these genomic regions through redundancy analysis. We found that the inversion exhibits broadly different patterns of divergence among annual and perennial M. guttatus and is associated with environmental variation across population accessions. This study is the first widespread population genetic survey of the diversity of the M. guttatus species complex. Our findings contribute to a greater understanding of morphological, ecological, and genetic evolutionary divergence across this highly diverse group of closely related ecotypes and species. Finally, understanding species relationships among M. guttatus sp. has hitherto been stymied by accumulated evidence of substantial gene flow among populations as well as designated species. Nevertheless, our results shed light on these relationships and provide insight into adaptation in life history traits within the complex.

opencc-zeroDec 2011View details →

Data from: Reproductive isolation and local adaptation quantified for a chromosome inversion in a malaria mosquito

Chromosome inversions have long been thought to be involved in speciation and local adaptation. We have little quantitative information, however, about the effects that inversion polymorphisms have on reproductive isolation and viability. Here we provide the first estimates from any organism for the total amount of reproductive isolation associated with an inversion segregating in natural populations. We sampled chromosomes from 751 mosquitoes of the malaria vector Anopheles funestus along a 1421 km transect in Cameroon that traverses savannah, highland, and rainforest ecological zones. We then developed a series of population genetic models that account for selection, migration, and assortative mating, and fit the models to the data using likelihood. Results from the best-fit models suggest there is strong local adaptation, with relative viabilities of homozygotes ranging from 25% to 130% compared to heterozygotes. Viabilities vary qualitatively between regions: the inversion is underdominant in the savannah, while in the highlands it is overdominant. The inversion is also implicated in strong assortative mating. In the savannah, the two homozygote forms show 92% reproductive isolation, suggesting that this one inversion can generate most of the genetic barriers needed for speciation.

opencc-zeroDec 2012View details →

Data from: Vanishing chromosomal inversion clines in Drosophila subobscura from Chile: is behavioral thermoregulation to blame?

Chromosomal inversion clines paralleling the long-standing ones in native Palearctic populations of Drosophila subobscura evolved swiftly after this species invaded the Americas in the late 1970s and early 1980s. However, the new clines did not consistently continue to converge on the Old World baseline. Our recent survey of Chilean populations of D. subobscura shows that inversion clines have faded or even changed sign with latitude. Here, we investigate the hypothesis that this fading of inversion clines might be due to the Bogert effect, namely, that flies' thermoregulatory behavior has eventually compensated for environmental variation in temperature, thus buffering selection on thermal-related traits. We show that latitudinal divergence in thermal preference (Tp) has evolved in Chile for females, with higher-latitude flies having a lower mean Tp. Plastic responses in Tp also lessen latitudinal thermal variation because flies developed at colder temperatures prefer warmer microclimates. Our results are consistent with the idea that active behavioral thermoregulation might buffer environmental variation and reduce the potential effect of thermal selection on other traits as chromosomal arrangements.

Data from: Empirical demonstration of hybrid chromosomal races in house mice

Western house mice (Mus musculus domesticus) and common shrews (Sorex araneus) are important models for study of chromosomal speciation. Both had ancestral karyotypes consisting of telocentric chromosomes, and each is subdivided into numerous chromosomal races many of which have resulted from fixation of new mutations (Robertsonian fusions and whole-arm reciprocal translocations). However, some chromosomal races in both species may alternatively have originated through hybridization, with particular homozygous recombinant products reaching fixation. Here, we demonstrate the process of generation of hybrid chromosomal races for the first time in either species using molecular markers. Analysis of centromeric microsatellite markers show that the Mid Valtellina (IMVA) and Upper Valtellina (IUVA) chromosomal races of the house mouse are recombinant products of hybridization of the Lower Valtellina (ILVA) and Poschiavo (CHPO) chromosomal races, supporting earlier theoretical analysis. IMVA and IUVA occupy a small area of the Italian Alps where ILVA makes contact with CHPO. IUVA and CHPO have previously been shown to be reproductively isolated in one village, emphasizing that hybrid chromosomal races in small mammals, as in plants, have the potential to be part of the speciation process.

Data from: Analysis of the karyotype structure in Ricolla quadrispinosa (Linneus, 1767): inferences about the chromosomal evolution of the tribes of Harpactorinae (Heteroptera, Reduviidae)

The subfamily Harpactorinae is composed of six tribes. Phylogenetic studies bring together some of Harpactorinae tribes, but by and large the data on evolutionary relationships of the subfamily are scarce. Chromosome studies are of great importance for understanding the systematics of different groups of insects. For Harpactorinae, these studies are restricted to some subfamilies and involved only conventional chromosome analysis. This work analyzed cytogenetically Ricolla quadrispinosa (Linneus, 1767). The chromosome number was determined as 2n = 24 + X1X2Y in males. In metaphase II the autosomal chromosomes were organized in a ring with the pseudo-trivalent of sex chromosomes in its center. After C-banding followed by staining with DAPI, AT-rich blocks in autosomes were observed and the negatively heteropycnotic sex chromosomes. The data obtained, together with existing data for other species of the group, indicated that different chromosomal rearrangements are involved in the evolution of the species. In addition, a proposal of karyotype evolution for the subfamily, based on existing phylogenetic studies for the group is presented.

opencc-zeroDec 2017View details →

Data from: Heterochromatin-enriched assemblies reveal the sequence and organization of the Drosophila melanogaster Y chromosome

Heterochromatic regions of the genome are repeat-rich and poor in protein coding genes, and are therefore underrepresented in even the best genome assemblies. One of the most difficult regions of the genome to assemble are sex-limited chromosomes. The Drosophila melanogaster Y chromosome is entirely heterochromatic, yet has wide-ranging effects on male fertility, fitness, and genome-wide gene expression. The genetic basis of this phenotypic variation is difficult to study, in part because we do not know the detailed organization of the Y chromosome. To study Y chromosome organization in D. melanogaster, we develop an assembly strategy involving the in silico enrichment of heterochromatic long single-molecule reads and use these reads to create targeted de novo assemblies of heterochromatic sequences. We assigned contigs to the Y chromosome using Illumina reads to identify male-specific sequences. Our pipeline extends the D. melanogaster reference genome by 11.9 Mb, closes 43.8% of the gaps, and improves overall contiguity. The addition of 10.6 MB of Y-linked sequence permitted us to study the organization of repeats and genes along the Y chromosome. We detected a high rate of duplication to the pericentric regions of the Y chromosome from other regions in the genome. Most of these duplicated genes exist in multiple copies. We detail the evolutionary history of one sex-linked gene family—crystal-Stellate. While the Y chromosome does not undergo crossing over, we observed high gene conversion rates within and between members of the crystal-Stellate gene family, Su(Ste), and PCKR, compared to genome-wide estimates. Our results suggest that gene conversion and gene duplication play an important role in the evolution of Y-linked genes.

Data from: The fire ant social chromosome supergene variant Sb shows low diversity but high divergence from SB

Variation in social behavior is common yet little is known about the genetic architectures underpinning its evolution. A rare exception is in the fire ant Solenopsis invicta: Alternative variants of a supergene region determine whether a colony will have exactly one or up to dozens of queens. The two variants of this region are carried by a pair of "social chromosomes", SB and Sb, which resemble a pair of sex chromosomes. Recombination is suppressed between the two chromosomes in the supergene region. While the X-like SB can recombine with itself in SB/SB queens, recombination is effectively absent in the Y-like Sb because Sb/Sb queens die before reproducing. Here, we analyze whole genome sequences of eight haploid SB males and eight haploid Sb males. We find extensive SB-Sb di↵erentiation throughout the >19Mb long supergene region. We find no evidence of "evolutionary strata" with different levels of divergence comparable to those reported in several sex chromosomes. A high proportion of substitutions between the SB and Sb haplotypes are nonsynonymous, suggesting inefficacy of purifying selection in Sb sequences, similar to that for Y-linked sequences in XY systems. Finally, we show that the Sb haplotype of the supergene region has 635-fold less nucleotide diversity than the rest of the genome. We discuss how this reduction could be due to a recent selective sweep affecting Sb specifically or associated with a population bottleneck during the invasion of North America by the sampled population.

opencc-zeroMay 2020View details →

Data from: Chromosome-level reference genome assembly and gene editing of the dead-leaf butterfly Kallima inachus

The leaf resemblance of Kallima (Nymphalidae) butterflies is an important ecological adaptive mechanism that increases survival. However, the genetic mechanism underlying ecological adaptation remains unclear owing to a dearth of genomic information. Herein, we revealed the karyotype (n = 31) of the dead-leaf butterfly Kallima inachus, assembled its high-quality chromosome-level reference genome (568.92 Mb; contig N50: 19.20 Mb), and identified its Z and candidate W chromosomes. To our knowledge, this is the first study to report on these aspects of this species. In the assembled genome, 15,309 protein-coding genes and 49.86% repeat elements were annotated. Phylogenetic analysis showed that K. inachus diverged from Melitaea cinxia (no leaf resemblance), both of which are in Nymphalinae, around 40 million years ago. Demographic analysis indicated that the effective population size of K. inachus decreased during the last interglacial period in the Pleistocene. The wings of adults with the pigmentary gene ebony knocked out using CRISPR/Cas9 showed phenotypes in which the orange dorsal region and entire ventral surface darkened, suggesting its vital role in the ecological adaption of dead-leaf butterflies. Our results provide important genome resources for investigating the genetic mechanism underlying protective resemblance in dead-leaf butterflies and insights into the molecular basis of protective coloration.

opencc-zeroDec 2018View details →

Data from: Chromosomal inversions in the Atlantic cod genome: implications for management of Canada's Northern cod stock

Following stock collapse and over twenty years of moratoria, the state of Canada's Northern Atlantic cod (Gadus morhua) remains precarious. To test if recent stock growth was of endogenous or exogenous origin, we performed a whole genome scan (ddRAD) on 135 adults captured in 2015 at three offshore spawning locations spanning the range of the offshore stock along the northeastern Newfoundland and Labrador shelf (Hawke Channel, Notre Dame Channel and Bonavista Corridor), with an additional 105 adults from three more southern locations (St. Anns Bank, Browns Bank and Bay of Fundy). Population structure analysis using 5,077 single nucleotide polymorphisms (SNPs) detected a distinct genetic break off the coast of Nova Scotia near 45 °N. Gene flow between groups north and south of this divide appears to be limited despite the presence of several northern-type and admixed individuals present in the southern area. North of the genetic divide, allele frequencies of neutral loci were indicative of a panmictic population. Several outlier SNPs were found to be associated with ecologically relevant physical characteristics (visual pigments, fin development, response to hypoxia, and various metabolic processes), which may be indicative of different ecological niches.

opencc-zeroDec 2017View details →

Data from: Opposing patterns of intraspecific and interspecific differentiation in sex chromosomes and autosomes

Linking intraspecific and interspecific divergence is an important challenge in speciation research. X chromosomes are expected to evolve faster than autosomes and disproportionately contribute to reproductive barriers, and comparing genetic variation on X and autosomal markers within and between species can elucidate evolutionary processes that shape genome variation. We performed RADseq on a 16-population transect of two closely-related Australian cricket species, Teleogryllus commodus and T. oceanicus, covering allopatry and sympatry. This classic study system for sexual selection provides a rare exception to Haldane's rule, as hybrid females are sterile. We found no evidence of recent introgression, despite the fact that the species co-exist in overlapping habitats in the wild and interbreed in the laboratory. Putative X-linked loci showed greater differentiation between species compared to autosomal loci. However, population differentiation within species was unexpectedly lower on X-linked markers than autosomal markers, and relative X-to-autosomal genetic diversity was inflated above neutral expectations. Populations of both species showed genomic signatures of recent population expansions, but these were not strong enough to account for the inflated X/A diversity. Instead, most of the excess polymorphism on the X could better be explained by sex-biased processes that increase the relative effective population size of the X, such as interspecific variation in the strength of sexual selection among males. Taken together, the opposing patterns of diversity and differentiation at X versus autosomal loci implicate a greater role for sex-linked genes in maintaining species boundaries in this system.

Data from: A novel locus on chromosome 1 underlies the evolution of a melanic plumage polymorphism in a wild songbird

Understanding the mechanisms responsible for phenotypic diversification within and among species ultimately rests with linking naturally occurring mutations to functionally and ecologically significant traits. Colour polymorphisms are of great interest in this context because discrete colour patterns within a population are often controlled by just a few genes in a common environment. We investigated how and why phenotypic diversity arose and persists in the Zosterops borbonicus white-eye of Reunion (Mascarene archipelago), a colour polymorphic songbird in which all highland populations contain individuals belonging to either a brown or a grey plumage morph. Using extensive phenotypic and genomic data, we demonstrate that this melanin-based colour polymorphism is controlled by a single locus on chromosome 1 with two large-effect alleles, which was not previously described as affecting hair or feather colour. Differences between colour morphs appear to rely upon complex cis-regulatory variation that either prevents the synthesis of pheomelanin in grey feathers, or increases its production in brown ones. We used coalescent analyses to show that, from a 'brown' ancestral population, the dominant 'grey' allele spread quickly once it arose from a new mutation. Since colour morphs are always found in mixture, this implies that the selected allele does not go to fixation, but instead reaches an intermediate frequency, as would be expected under balancing selection.

Data from: Cladogenetic and anagenetic models of chromosome number evolution: a Bayesian model averaging approach

Chromosome number is a key feature of the higher-order organization of the genome, and changes in chromosome number play a fundamental role in evolution. Dysploid gains and losses in chromosome number, as well as polyploidization events, may drive reproductive isolation and lineage diversification. The recent development of probabilistic models of chromosome number evolution in the groundbreaking work by Mayrose et al. (2010, ChromEvol) have enabled the inference of ancestral chromosome numbers over molecular phylogenies and generated new interest in studying the role of chromosome changes in evolution. However, the ChromEvol approach assumes all changes occur anagenetically (along branches), and does not model events that are specifically cladogenetic. Cladogenetic changes may be expected if chromosome changes result in reproductive isolation. Here we present a new class of models of chromosome number evolution (called ChromoSSE) that incorporate both anagenetic and cladogenetic change. The ChromoSSE models allow us to determine the mode of chromosome number evolution; is chromosome evolution occurring primarily within lineages, primarily at lineage splitting, or in clade-specific combinations of both? Furthermore, we can estimate the location and timing of possible chromosome speciation events over the phylogeny. We implemented ChromoSSE in a Bayesian statistical framework, specifically in the software RevBayes, to accommodate uncertainty in parameter estimates while leveraging the full power of likelihood based methods. We tested ChromoSSE's accuracy with simulations and re-examined chromosomal evolution in Aristolochia, Carex section Spirostachyae, Helianthus, Mimulus sensu lato (s.l.), and Primula section Aleuritia, finding evidence for clade-specific combinations of anagenetic and cladogenetic dysploid and polyploid modes of chromosome evolution.

opencc-zeroDec 2014View details →

Data from: Chromosomal patterns of diversity and differentiation in creepers: a next-gen phylogeographic investigation of Certhia americana

With methods for sequencing thousands of loci for many individuals, phylogeographic studies have increased inferential power and the potential for applications to new questions. In songbirds, strong patterns of inter-chromosomal synteny, the published genome of a songbird and the ability to obtain thousands of genetic loci for many individuals permit the investigation of differentiation between and diversity within lineages across chromosomes. Here, we investigate patterns of differentiation and diversity in Certhia americana, a widespread North American songbird, using next-generation sequencing. Additionally, we reassess previous phylogeographic studies within the group. Based on ~30 million sequencing reads and more than 16 000 single-nucleotide polymorphisms in 41 individuals, we identified a strong positive relationship between genetic differentiation and chromosome size, with a negative relationship between genetic diversity and chromosome size. A combination of selection and drift may explain these patterns, although we found no evidence for selection. Because the observed genomic patterns are very similar between widespread, allopatric clades, it is unlikely that selective pressures would be so similar across such different ecological conditions. Alternatively, the accumulation of fixed differences between lineages and loss of genetic variation within lineages due to genetic drift alone may explain the observed patterns. Due to relatively higher recombination rates on smaller chromosomes, larger chromosomes would, on average, accumulate fixed differences between lineages and lose genetic variation within lineages faster, leading to the patterns observed here in C. americana.