Showing papers in "Journal of Heredity in 2020"

Comparing Adaptive Radiations Across Space, Time, and Taxa

Abstract: Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalities among disparate examples, ranging from plants to invertebrate and vertebrate animals, and remote islands to lakes and continents, to better understand processes shared across adaptive radiations. We surveyed many groups to evaluate factors considered important in a large variety of species radiations. In each of these studies, ecological opportunity of some form is identified as a prerequisite for adaptive radiation. However, evolvability, which can be enhanced by hybridization between distantly related species, may play a role in seeding entire radiations. Within radiations, the processes that lead to speciation depend largely on (1) whether the primary drivers of ecological shifts are (a) external to the membership of the radiation itself (mostly divergent or disruptive ecological selection) or (b) due to competition within the radiation membership (interactions among members) subsequent to reproductive isolation in similar environments, and (2) the extent and timing of admixture. These differences translate into different patterns of species accumulation and subsequent patterns of diversity across an adaptive radiation. Adaptive radiations occur in an extraordinary diversity of different ways, and continue to provide rich data for a better understanding of the diversification of life.

ILS-Aware Analysis of Low-Homoplasy Retroelement Insertions: Inference of Species Trees and Introgression Using Quartets.

Abstract: DNA sequence alignments have provided the majority of data for inferring phylogenetic relationships with both concatenation and coalescent methods. However, DNA sequences are susceptible to extensive homoplasy, especially for deep divergences in the Tree of Life. Retroelement insertions have emerged as a powerful alternative to sequences for deciphering evolutionary relationships because these data are nearly homoplasy-free. In addition, retroelement insertions satisfy the "no intralocus-recombination" assumption of summary coalescent methods because they are singular events and better approximate neutrality relative to DNA loci commonly sampled in phylogenomic studies. Retroelements have traditionally been analyzed with parsimony, distance, and network methods. Here, we analyze retroelement data sets for vertebrate clades (Placentalia, Laurasiatheria, Balaenopteroidea, Palaeognathae) with 2 ILS-aware methods that operate by extracting, weighting, and then assembling unrooted quartets into a species tree. The first approach constructs a species tree from retroelement bipartitions with ASTRAL, and the second method is based on split-decomposition with parsimony. We also develop a Quartet-Asymmetry test to detect hybridization using retroelements. Both ILS-aware methods recovered the same species-tree topology for each data set. The ASTRAL species trees for Laurasiatheria have consecutive short branch lengths in the anomaly zone whereas Palaeognathae is outside of this zone. For the Balaenopteroidea data set, which includes rorquals (Balaenopteridae) and gray whale (Eschrichtiidae), both ILS-aware methods resolved balaeonopterids as paraphyletic. Application of the Quartet-Asymmetry test to this data set detected 19 different quartets of species for which historical introgression may be inferred. Evidence for introgression was not detected in the other data sets.

Consequences of Single-Locus and Tightly Linked Genomic Architectures for Evolutionary Responses to Environmental Change.

Abstract: Genetic and genomic architectures of traits under selection are key factors influencing evolutionary responses. Yet, knowledge of their impacts has been limited by a widespread assumption that most traits are controlled by unlinked polygenic architectures. Recent advances in genome sequencing and eco-evolutionary modeling are unlocking the potential for integrating genomic information into predictions of population responses to environmental change. Using eco-evolutionary simulations, we demonstrate that hypothetical single-locus control of a life history trait produces highly variable and unpredictable harvesting-induced evolution relative to the classically applied multilocus model. Single-locus control of complex traits is thought to be uncommon, yet blocks of linked genes, such as those associated with some types of structural genomic variation, have emerged as taxonomically widespread phenomena. Inheritance of linked architectures resembles that of single loci, thus enabling single-locus-like modeling of polygenic adaptation. Yet, the number of loci, their effect sizes, and the degree of linkage among them all occur along a continuum. We review how linked architectures are often associated, directly or indirectly, with traits expected to be under selection from anthropogenic stressors and are likely to play a large role in adaptation to environmental disturbance. We suggest using single-locus models to explore evolutionary extremes and uncertainties when the trait architecture is unknown, refining parameters as genomic information becomes available, and explicitly incorporating linkage among loci when possible. By overestimating the complexity (e.g., number of independent loci) of the genomic architecture of traits under selection, we risk underestimating the complexity (e.g., nonlinearity) of their evolutionary dynamics.

First report of sex chromosomes in night lizards (Scincoidea: Xantusiidae).

Abstract: Squamate reptiles (lizards, snakes, and amphibians) are an outstanding group for studying sex chromosome evolution-they are old, speciose, geographically widespread, and exhibit myriad sex-determining modes. Yet, the vast majority of squamate species lack heteromorphic sex chromosomes. Cataloging the sex chromosome systems of species lacking easily identifiable, heteromorphic sex chromosomes, therefore, is essential before we are to fully understand the evolution of vertebrate sex chromosomes. Here, we use restriction site-associated DNA sequencing (RADseq) to classify the sex chromosome system of the granite night lizard, Xantusia henshawi. RADseq is an effective alternative to traditional cytogenetic methods for determining a species' sex chromosome system (i.e., XX/XY or ZZ/ZW), particularly in taxa with non-differentiated sex chromosomes. Although many xantusiid lineages have been karyotyped, none possess heteromorphic sex chromosomes. We identified a ZZ/ZW sex chromosome system in X. henshawi-the first such data for this family. Furthermore, we report that the X. henshawi sex chromosome contains fragments of genes found on Gallus gallus chromosomes 7, 12, and 18 (which are homologous to Anolis carolinensis chromosome 2), the first vertebrate sex chromosomes to utilize this linkage group.

Insights into the Evolutionary History of the Hawaiian Bidens (Asteraceae) Adaptive Radiation Revealed Through Phylogenomics

Abstract: Hawaiian plant radiations often result in lineages with exceptionally high species richness and extreme morphological and ecological differentiation. However, they typically display low levels of genetic variation, hindering the use of classic DNA markers to resolve their evolutionary histories. Here we utilize a phylogenomic approach to generate the first generally well-resolved phylogenetic hypothesis for the evolution of the Hawaiian Bidens (Asteraceae) adaptive radiation, including refined initial colonization and divergence time estimates. We sequenced the chloroplast genome (plastome) and nuclear ribosomal complex for 18 of the 19 endemic species of Hawaiian Bidens and 4 outgroup species. Phylogenomic analyses based on the concatenated dataset (plastome and nuclear) resulted in identical Bayesian and Maximum Likelihood trees with high statistical support at most nodes. Estimates from dating analyses were similar across datasets, with the crown group emerging ~1.76-1.82 Mya. Biogeographic analyses based on the nuclear and concatenated datasets indicated that colonization within the Hawaiian Islands generally followed the progression rule with 67-80% of colonization events from older to younger islands, while only 53% of events followed the progression rule in the plastome analysis. We find strong evidence for nuclear-plastome conflict indicating a potentially important role for hybridization in the evolution of the group. However, incomplete lineage sorting cannot be ruled out due to the small number of independent loci analyzed. This study contributes new insights into species relationships and the biogeographic history of the explosive Hawaiian Bidens adaptive radiation.

Bridging the Process-Pattern Divide to Understand the Origins and Early Stages of Adaptive Radiation: A Review of Approaches With Insights From Studies of Anolis Lizards

Abstract: Understanding the origins and early stages of diversification is one of the most elusive tasks in adaptive radiation research. Classical approaches, which aim to infer past processes from present-day patterns of biological diversity, are fraught with difficulties and assumptions. An alternative approach has been to study young clades of relatively few species, which may represent the putative early stages of adaptive radiation. However, it is difficult to predict whether those groups will ever reach the ecological and morphological disparity observed in the sorts of clades usually referred to as adaptive radiations, thereby making their utility in informing the early stages of such radiations uncertain. Caribbean Anolis lizards are a textbook example of an adaptive radiation; anoles have diversified independently on each of the 4 islands in the Greater Antilles, producing replicated radiations of phenotypically diverse species. However, the underlying processes that drove these radiations occurred 30-65 million years ago and so are unobservable, rendering major questions about how these radiations came to be difficult to tackle. What did the ancestral species of the anole radiation look like? How did new species arise? What processes drove adaptive diversification? Here, we review what we have learned about the cryptic early stages of adaptive radiation from studies of Anolis lizards, and how these studies have attempted to bridge the process-pattern divide of adaptive radiation research. Despite decades of research, however, fundamental questions linking eco-evolutionary processes to macroevolutionary patterns in anoles remain difficult to answer.

Species Radiations in the Sea: What the Flock?

Abstract: Species flocks are proliferations of closely-related species, usually after colonization of depauperate habitat. These radiations are abundant on oceanic islands and in ancient freshwater lakes, but rare in marine habitats. This contrast is well documented in the Hawaiian Archipelago, where terrestrial examples include the speciose silverswords (sunflower family Asteraceae), Drosophila fruit flies, and honeycreepers (passerine birds), all derived from one or a few ancestral lineages. The marine fauna of Hawai'i is also the product of rare colonization events, but these colonizations usually yield only one species. Dispersal ability is key to understanding this evolutionary inequity. While terrestrial fauna rarely colonize between oceanic islands, marine fauna with pelagic larvae can make this leap in every generation. An informative exception is the marine fauna that lack a pelagic larval stage. These low-dispersal species emulate a "terrestrial" mode of reproduction (brooding, viviparity, crawl-away larvae), yielding marine species flocks in scattered locations around the world. Elsewhere, aquatic species flocks are concentrated in specific geographic settings, including the ancient lakes of Baikal (Siberia) and Tanganyika (eastern Africa), and Antarctica. These locations host multiple species flocks across a broad taxonomic spectrum, indicating a unifying evolutionary phenomenon. Hence marine species flocks can be singular cases that arise due to restricted dispersal or other intrinsic features, or they can be geographically clustered, promoted by extrinsic ecological circumstances. Here, we review and contrast intrinsic cases of species flocks in individual taxa, and extrinsic cases of geological/ecological opportunity, to elucidate the processes of species radiations.

A Genome-Wide Perspective on the Persistence of Red Wolf Ancestry in Southeastern Canids

Abstract: The red wolf (Canis rufus), a legally recognized and critically endangered wolf, is known to interbreed with coyotes (Canis latrans). Declared extirpated in the wild in 1980, red wolves were reintroduced to northeastern North Carolina nearly a decade later. Interbreeding with coyotes was thought to be restricted to a narrow geographic region adjacent to the reintroduced population and largely believed to threaten red wolf recovery. However, red wolf ancestry was recently discovered in canids along the American Gulf Coast, igniting a broader survey of ancestry in southeastern canid populations. Here, we examine geographic and temporal patterns of genome-wide red wolf ancestry in 260 canids across the southeastern United States at over 164 000 SNP loci. We found that red wolf ancestry was most prevalent in canids sampled from Texas in the mid-1970s, although non-trivial amounts of red wolf ancestry persist in this region today. Further, red wolf ancestry was also observed in a subset of coyotes inhabiting North Carolina, despite management efforts to limit the occurrence of hybridization events. Lastly, we found no evidence of substantial red wolf ancestry in southeastern canids outside of these 2 admixture zones. Overall, this study provides a genome-wide survey of red wolf ancestry in canids across the southeastern United States, which may ultimately inform future red wolf restoration efforts.

Genetic Diversity and Connectivity of Southern Right Whales (Eubalaena australis) Found in the Brazil and Chile-Peru Wintering Grounds and the South Georgia (Islas Georgias del Sur) Feeding Ground.

Abstract: As species recover from exploitation, continued assessments of connectivity and population structure are warranted to provide information for conservation and management. This is particularly true in species with high dispersal capacity, such as migratory whales, where patterns of connectivity could change rapidly. Here we build on a previous long-term, large-scale collaboration on southern right whales (Eubalaena australis) to combine new (nnew) and published (npub) mitochondrial (mtDNA) and microsatellite genetic data from all major wintering grounds and, uniquely, the South Georgia (Islas Georgias del Sur: SG) feeding grounds. Specifically, we include data from Argentina (npub mtDNA/microsatellite = 208/46), Brazil (nnew mtDNA/microsatellite = 50/50), South Africa (nnew mtDNA/microsatellite = 66/77, npub mtDNA/microsatellite = 350/47), Chile-Peru (nnew mtDNA/microsatellite = 1/1), the Indo-Pacific (npub mtDNA/microsatellite = 769/126), and SG (npub mtDNA/microsatellite = 8/0, nnew mtDNA/microsatellite = 3/11) to investigate the position of previously unstudied habitats in the migratory network: Brazil, SG, and Chile-Peru. These new genetic data show connectivity between Brazil and Argentina, exemplified by weak genetic differentiation and the movement of 1 genetically identified individual between the South American grounds. The single sample from Chile-Peru had an mtDNA haplotype previously only observed in the Indo-Pacific and had a nuclear genotype that appeared admixed between the Indo-Pacific and South Atlantic, based on genetic clustering and assignment algorithms. The SG samples were clearly South Atlantic and were more similar to the South American than the South African wintering grounds. This study highlights how international collaborations are critical to provide context for emerging or recovering regions, like the SG feeding ground, as well as those that remain critically endangered, such as Chile-Peru.

Archipelago-Wide Patterns of Colonization and Speciation Among an Endemic Radiation of Galápagos Land Snails.

Abstract: Newly arrived species on young or remote islands are likely to encounter less predation and competition than source populations on continental landmasses. The associated ecological release might facilitate divergence and speciation as colonizing lineages fill previously unoccupied niche space. Characterizing the sequence and timing of colonization on islands represents the first step in determining the relative contributions of geographical isolation and ecological factors in lineage diversification. Herein, we use genome-scale data to estimate timing of colonization in Naesiotus snails to the Galapagos islands from mainland South America. We test inter-island patterns of colonization and within-island radiations to understand their contribution to community assembly. Partly contradicting previously published topologies, phylogenetic reconstructions suggest that most Naesiotus species form island-specific clades, with within-island speciation dominating cladogenesis. Galapagos Naesiotus also adhere to the island progression rule, with colonization proceeding from old to young islands and within-island diversification occurring earlier on older islands. Our work provides a framework for evaluating the contribution of colonization and in situ speciation to the diversity of other Galapagos lineages.

Genetic Diversity and Population Structure of Dromedary Camel-Types

Abstract: The dromedary camel is a unique livestock for its adaptations to arid-hot environments and its ability to provide goods under extreme conditions. There are no registries or breed standards for camels. Thus, named camel populations (i.e., camel-types) were examined for genetic uniqueness and breed status. Camel populations are generally named based on shared phenotype, country or region of origin, tribal ownership, or the ecology of their habitat. A dataset of 10 Short-Tandem Repeat markers genotyped for 701 individual camels from 27 camel-types was used to quantify genetic diversity within camel-types, compare genetic diversity across camel-types, determine the population genetic structure of camel-types, and identify camel-types that may represent true breeds. Summary statistics (genotyping call rate, heterozygosity, inbreeding coefficient FIS, and allelic frequencies) were calculated and population-specific analyses (pairwise FST, neighbor-joining tree, relatedness, Nei's genetic distance, principal coordinate analysis [PCoA], and STRUCTURE) were performed. The most notable findings were 1) little variation in genetic diversity was found across the camel-types, 2) the highest genetic diversity measure was detected in Targui and the lowest was in Awarik, 3) camel-types from Asia (especially the Arabian Peninsula) exhibited higher genetic diversity than their counterparts in Africa, 4) the highest DeltaK value of population structure separated camel-types based on geography (Asia vs. Africa), 5) the most distinct camel-types were the Omani, Awarik, and the Gabbra, 6) camel-types originating from the same country did not necessarily share high genetic similarity (e.g., camel-types from Oman), and 7) camel-type names were not consistently indicative of breed status.

Reinforcement and the Proliferation of Species.

Abstract: Adaptive radiations are characterized by the rapid proliferation of species. Explaining how adaptive radiations occur therefore depends, in part, on identifying how populations become reproductively isolated-and ultimately become different species. Such reproductive isolation could arise when populations adapting to novel niches experience selection to avoid interbreeding and, consequently, evolve mating traits that minimize such hybridization via the process of reinforcement. Here, we highlight that a downstream consequence of reinforcement is divergence of conspecific populations, and this further divergence can instigate species proliferation. Moreover, we evaluate when reinforcement will-and will not-promote species proliferation. Finally, we discuss empirical approaches to test what role, if any, reinforcement plays in species proliferation and, consequently, in adaptive radiation. To date, reinforcement's downstream effects on species proliferation remain largely unknown and speculative. Because the ecological and evolutionary contexts in which adaptive radiations occur are conducive to reinforcement and its downstream consequences, adaptive radiations provide an ideal framework in which to evaluate reinforcement's role in diversification.

Isolation of Metrosideros (ʻOhiʻa) Taxa on Oʻahu Increases with Elevation and Extreme Environments

Abstract: Species radiations should be facilitated by short generation times and limited dispersal among discontinuous populations. Hawaii's hyper-diverse, landscape-dominant tree, Metrosideros, is unique among the islands' radiations for its massive populations that occur continuously over space and time within islands, its exceptional capacity for gene flow by both pollen and seed, and its extended life span (ca. >650 years). Metrosideros shows the greatest phenotypic and microsatellite DNA diversity on O'ahu, where taxa occur in tight sympatry or parapatry in mesic and montane wet forest on 2 volcanoes. We document the nonrandom distributions of 12 taxa (including unnamed morphotypes) along elevation gradients, measure phenotypes of ~6-year-old common-garden plants of 8 taxa to verify heritability of phenotypes, and examine genotypes of 476 wild adults at 9 microsatellite loci to compare the strengths of isolation across taxa, volcanoes, and distance. All 8 taxa retained their diagnostic phenotypes in the common garden. Populations were isolated by taxon to a range of degrees (pairwise FST between taxa: 0.004-0.267), and there was no pattern of isolation by distance or by elevation; however, significant isolation between volcanoes was observed within monotypic species, suggesting limited gene flow between volcanoes. Among the infraspecific taxa of Metrosideros polymorpha, genetic diversity and isolation significantly decreased and increased, respectively, with elevation. Overall, 5 of the 6 most isolated taxa were associated with highest elevations or otherwise extreme environments. These findings suggest a principal role for selection in the origin and maintenance of the exceptional diversity that occurs within continuous Metrosideros stands on O'ahu.

Genomic Footprints of Recovery in the European Bison.

Abstract: After extinction in the wild in the beginning of the 20th century, the European bison has been successfully recovered in 2 distinct genetic lines from only 12 and 7 captive founders. We here aimed at characterizing the levels of realized inbreeding in these 2 restored lines to provide empirical insights into the genomic footprints left by population recovery from a small number of founders. To that end, we genotyped 183 European bison born over the last 40 years with the Illumina BovineHD beadchip that contained 22 602 informative autosomal single-nucleotide polymorphisms after data filtering. We then identified homozygous-by-descent (HBD) segments and classified them into different age-related classes relying on a model-based approach. As expected, we observed that the strong and recent founder effect experienced by the 2 lines resulted in very high levels of recent inbreeding and in the presence of long HBD tracks (up to 120 Mb). These long HBD tracks were associated with ancestors living approximately from 4 to 32 generations in the past, suggesting that inbreeding accumulated over multiple generations after the bottleneck. The contribution to inbreeding of the most recent groups of ancestors was however found to be decreasing in both lines. In addition, comparison of Lowland individuals born at different time periods showed that the levels of inbreeding tended to stabilize, HBD segments being shorter in animals born more recently which indicates efficient control of inbreeding. Monitoring HBD segment lengths over generations may thus be viewed as a valuable genomic diagnostic tool for populations in conservation or recovery programs.

The influence of environmental variation on the genetic structure of a poison frog distributed across continuous Amazonian rainforest

Abstract: Biogeographic barriers such as rivers have been shown to shape spatial patterns of biodiversity in the Amazon basin, yet relatively little is known about the distribution of genetic variation across continuous rainforest. Here, we characterize the genetic structure of the brilliant-thighed poison frog (Allobates femoralis) across an 880 km long transect along the Purus-Madeira interfluve south of the Amazon river, based on 64 individuals genotyped at 7 609 SNP loci. A population tree and clustering analyses revealed four distinct genetic groups, one of which was strongly divergent. These genetic groups were concomitant with femoral spot coloration differences, which was intermediate within a zone of admixture between two of the groups. The location of these genetic groups did not consistently correspond to current ecological transitions between major forest types. A multi-model approach to quantify the relative influence of isolation-by-distance (IBD) and isolation-by-environmental resistance (IBR) nevertheless revealed that, in addition to a strong signal of IBD, spatial genetic differentiation was explained by IBR primarily linked to dry season intensity (r 2 = 8.4%) and canopy cover (r 2 = 6.4%). We show significant phylogenetic divergence in the absence of obvious biogeographical barriers and that finer-scaled measures of genetic structure show patterns that are associated with environmental variables also known to predict the density of A. femoralis.

The estrogen-responsive transcriptome of female secondary sexual traits in the Gulf pipefish.

Abstract: Sexual dimorphism often results from hormonally regulated trait differences between the sexes. In sex-role-reversed vertebrates, females often have ornaments used in mating competition that are expected to be under hormonal control. Males of the sex-role-reversed Gulf pipefish (Syngnathus scovelli) develop female-typical traits when they are exposed to estrogens. We aimed to identify genes whose expression levels changed during the development and maintenance of female-specific ornaments. We performed RNA-sequencing on skin and muscle tissue in male Gulf pipefish with and without exposure to estrogen to investigate the transcriptome of the sexually dimorphic ornament of vertical iridescent bands found in females and estrogen-exposed males. We further compared differential gene expression patterns between males and females to generate a list of genes putatively involved in the female secondary sex traits of bands and body depth. A detailed analysis of estrogen-receptor binding sites demonstrates that estrogen-regulated genes tend to have nearby cis-regulatory elements. Our results identified a number of genes that differed between the sexes and confirmed that many of these were estrogen-responsive. These estrogen-regulated genes may be involved in the arrangement of chromatophores for color patterning, as well as in the growth of muscles to achieve the greater body depth typical of females in this species. In addition, anaerobic respiration and adipose tissue could be involved in the rigors of female courtship and mating competition. Overall, this study generates a number of interesting hypotheses regarding the genetic basis of a female ornament in a sex-role-reversed pipefish.

New Genetic Insights About Hybridization and Population Structure of Hawksbill and Loggerhead Turtles From Brazil.

Abstract: An extremely high incidence of hybridization among sea turtles is found along the Brazilian coast. This atypical phenomenon and its impact on sea turtle conservation can be elucidated through research focused on the evolutionary history of sea turtles. We assessed high-quality multilocus haplotypes of 143 samples of the 5 species of sea turtles that occur along the Brazilian coast to investigate the hybridization process and the population structure of hawksbill (Eretmochelys imbricata) and loggerhead turtles (Caretta caretta). The multilocus data were initially used to characterize interspecific hybrids. Introgression (F2 hybrids) was only confirmed in hatchlings of F1 hybrid females (hawksbill × loggerhead), indicating that introgression was either previously overestimated and F2 hybrids may not survive to adulthood, or the first-generation hybrid females nesting in Brazil were born as recent as few decades ago. Phylogenetic analyses using nuclear markers recovered the mtDNA-based Indo-Pacific and Atlantic lineages for hawksbill turtles, demonstrating a deep genetic divergence dating from the early Pliocene. In addition, loggerhead turtles that share a common feeding area and belong to distinct Indo-Pacific and Atlantic mtDNA clades present no clear genetic differentiation at the nuclear level. Finally, our results indicate that hawksbill and loggerhead rookeries along the Brazilian coast are likely connected by male-mediated gene flow.

Updating the Bibliography of Interbreeding among Canis in North America.

Abstract: This bibliography provides a collection of references that documents the evolution of studies evidencing interbreeding among Canis species in North America. Over the past several decades, advances in biology and genomic technology greatly improved our ability to detect and characterize species interbreeding, which has significance for understanding species in a changing landscape as well as for endangered species management. This bibliography includes a discussion within each category of interbreeding, the timeline of developing evidence, and includes a review of past research conducted on experimental crosses. Research conducted in the early 20th century is rich with detailed records and photographs of hybrid offspring development and behavior. With the progression of molecular methods, studies can estimate historical demographic parameters and detect chromosomal patterns of ancestry. As these methods continue to increase in accessibility, the field will gain a deeper and richer understanding of the evolutionary history of North American Canis.

Intraspecific Genetic Variation Underlying Postmating Reproductive Barriers between Species in the Wild Tomato Clade (Solanum sect. Lycopersicon)

Abstract: A goal of speciation genetics is to understand how the genetic components underlying interspecific reproductive barriers originate within species. Unilateral incompatibility (UI) is a postmating prezygotic barrier in which pollen rejection in the female reproductive tract (style) occurs in only one direction of an interspecific cross. Natural variation in the strength of UI has been observed among populations within species in the wild tomato clade. In some cases, molecular loci underlying self-incompatibility (SI) are associated with this variation in UI, but the mechanistic connection between these intra- and inter-specific pollen rejection behaviors is poorly understood in most instances. We generated an F2 population between SI and SC genotypes of a single species, Solanum pennellii, to examine the genetic basis of intraspecific variation in UI against other species, and to determine whether loci underlying SI are genetically associated with this variation. We found that F2 individuals vary in the rate at which UI rejection occurs. One large effect QTL detected for this trait co-localized with the SI-determining S-locus. Moreover, individuals that expressed S-RNase-the S-locus protein involved in SI pollen rejection-in their styles had much more rapid UI responses compared with those without S-RNase protein. Our analysis shows that intraspecific variation at mate choice loci-in this case at loci that prevent self-fertilization-can contribute to variation in the expression of interspecific isolation, including postmating prezygotic barriers. Understanding the nature of such intraspecific variation can provide insight into the accumulation of these barriers between diverging lineages.

Disentangling Complex Inheritance Patterns of Plant Organellar Genomes: An Example From Carrot.

Abstract: Plant mitochondria and plastids display an array of inheritance patterns and varying levels of heteroplasmy, where individuals harbor more than 1 version of a mitochondrial or plastid genome. Organelle inheritance in plants has the potential to be quite complex and can vary with plant growth, development, and reproduction. Few studies have sought to investigate these complicated patterns of within-individual variation and inheritance using experimental crosses in plants. We carried out crosses in carrot, Daucus carota L. (Apiaceae), which has previously been shown to exhibit organellar heteroplasmy. We used mitochondrial and plastid markers to begin to disentangle the patterns of organellar inheritance and the fate of heteroplasmic variation, with special focus on cases where the mother displayed heteroplasmy. We also investigated heteroplasmy across the plant, assaying leaf samples at different development stages and ages. Mitochondrial and plastid paternal leakage was rare and offspring received remarkably similar heteroplasmic mixtures to their heteroplasmic mothers, indicating that heteroplasmy is maintained over the course of maternal inheritance. When offspring did differ from their mother, they were likely to exhibit a loss of the genetic variation that was present in their mother. Finally, we found that mitochondrial variation did not vary significantly over plant development, indicating that substantial vegetative sorting did not occur. Our study is one of the first to quantitatively investigate inheritance patterns and heteroplasmy in plants using controlled crosses, and we look forward to future studies making use of whole genome information to study the complex evolutionary dynamics of plant organellar genomes.

Prion Protein Gene (PRNP) Sequences Suggest Differing Vulnerability to Chronic Wasting Disease for Florida Key Deer (Odocoileus virginianus clavium) and Columbian White-Tailed Deer (O. v. leucurus).

Abstract: Chronic wasting disease (CWD) is a fatal, highly transmissible spongiform encephalopathy caused by an infectious prion protein. CWD is spreading across North American cervids. Studies of the prion protein gene (PRNP) in white-tailed deer (WTD; Odocoileus virginianus) have identified non-synonymous substitutions associated with reduced CWD frequency. Because CWD is spreading rapidly geographically, it may impact cervids of conservation concern. Here, we examined the genetic vulnerability to CWD of 2 subspecies of WTD: the endangered Florida Key deer (O. v. clavium) and the threatened Columbian WTD (O. v. leucurus). In Key deer (n = 48), we identified 3 haplotypes formed by 5 polymorphisms, of which 2 were non-synonymous. The polymorphism c.574G>A, unique to Key deer (29 of 96 chromosomes), encodes a non-synonymous substitution from valine to isoleucine at codon 192. In 91 of 96 chromosomes, Key deer carried c.286G>A (G96S), previously associated with substantially reduced susceptibility to CWD. Key deer may be less genetically susceptible to CWD than many mainland WTD populations. In Columbian WTD (n = 13), 2 haplotypes separated by one synonymous substitution (c.438C>T) were identified. All of the Columbian WTD carried alleles that in other mainland populations are associated with relatively high susceptibility to CWD. While larger sampling is needed, future management plans should consider that Columbian WTD are likely to be genetically more vulnerable to CWD than many other WTD populations. Finally, we suggest that genetic vulnerability to CWD be assessed by sequencing PRNP across other endangered cervids, both wild and in captive breeding facilities.

Allele-Specific Expression and Evolution of Gene Regulation Underlying Acute Heat Stress Response and Local Adaptation in the Copepod Tigriopus californicus.

Abstract: Geographic variation in environmental temperature can select for local adaptation among conspecific populations. Divergence in gene expression across the transcriptome is a key mechanism for evolution of local thermal adaptation in many systems, yet the genetic mechanisms underlying this regulatory evolution remain poorly understood. Here we examine gene expression in 2 locally adapted Tigriopus californicus populations (heat tolerant San Diego, SD, and less tolerant Santa Cruz, SC) and their F1 hybrids during acute heat stress response. Allele-specific expression (ASE) in F1 hybrids was used to determine cis-regulatory divergence. We found that the number of genes showing significant allelic imbalance increased under heat stress compared to unstressed controls. This suggests that there is significant population divergence in cis-regulatory elements underlying heat stress response. Specifically, the number of genes showing an excess of transcripts from the more thermal tolerant (SD) population increased with heat stress while that number of genes with an SC excess was similar in both treatments. Inheritance patterns of gene expression also revealed that genes displaying SD-dominant expression phenotypes increase in number in response to heat stress; that is, across loci, gene expression in F1's following heat stress showed more similarity to SD than SC, a pattern that was absent in the control treatment. The observed patterns of ASE and inheritance of gene expression provide insight into the complex processes underlying local adaptation and thermal stress response.

A De Novo MITF Deletion Explains a Novel Splashed White Phenotype in an American Paint Horse.

Abstract: Splashed white is a coat color pattern in horses characterized by extensive white patterning on the legs, belly, and face often accompanied by blue eyes and deafness. Three mutations in microphthalmia-associated transcription factor (MITF) and two mutations in Paired Box 3 (PAX3) have been identified that explain splashed white patterns (SW1-SW5). An American Paint Horse stallion with a splashed white phenotype and blue eyes, whose parents were not white patterned, was negative for the 5 known splashed white variants and other known white spotting alleles. This novel splashed white phenotype (SW6) was hypothesized to be caused by a de novo mutation in MITF or PAX3. Analysis of whole-genome sequencing using the EquCab3.0 reference genome for comparison identified an 8.7 kb deletion in MITF on ECA16 (NC_009159.3:g.21551060-21559770del). The deletion encompassed part of intron 7 through the 3' UTR of exon 9 of MITF, including the helix-loop-helix DNA-binding domain (ENSECAT00000006375.3). This variant is predicted to truncate protein and impair binding to DNA. Sanger sequencing confirmed the stallion was heterozygous for the MITF deletion. No single nucleotide polymorphisms (SNPs) or structural variants were identified in PAX3 or any of the other candidate genes that were unique to the stallion or predicted to affect protein function. Genotyping five of the stallion's splashed white offspring, including one all white foal, found that they were also heterozygous for the deletion. Given the role of MITF in producing white pattern phenotypes, and the predicted deleterious effect of this mutation, this 8.7 kb deletion is the likely causal variant for SW6.

Macroevolutionary Patterns of Sexual Size Dimorphism Among African Tree Frogs (Family: Hyperoliidae)

Abstract: Sexual size dimorphism (SSD) is shaped by multiple selective forces that drive the evolution of sex-specific body size, resulting in male or female-biased SSD Stronger selection on one sex can result in an allometric body size scaling relationship consistent with Rensch's rule or its converse Anurans (frogs and toads) generally display female-biased SSD, but there is variation across clades and the mechanisms driving the evolution of SSD remain poorly understood We investigated these topics in a diverse family of African treefrogs (Hyperoliidae) Hyperoliids display traits considered rare among amphibians, including sexual dichromatism and protogynous sex change Using phylogenetic comparative methods, we tested if adult ecology, sexual dichromatism, and sex change were predictors of body size or SSD We also tested whether hyperoliids displayed allometric interspecific body size scaling relationships We found a majority of hyperoliid taxa display female-biased SSD, but that adult ecology and sexual dichromatism are poor predictors of sex-specific body size and SSD Regardless of the groupings analyzed (partitioned by clades or traits), we found support for isometric body size scaling However, we found that sex change is a significant predictor of SSD variation Species in the Hyperolius viridiflavus complex, which putatively display this trait, show a significant reduction in SSD and are frequently sexually monomorphic in size Although protogynous sex change needs to be validated for several of these species, we tentatively propose this trait is a novel mechanism influencing anuran body size evolution Beyond this association, additional factors that shape the evolution of anuran body size and SSD remain elusive

Mitogenomes Reveal Multiple Colonization of Mountains by Rattus in Sundaland.

Abstract: Tropical mountains are cradles of biodiversity and endemism. Sundaland, tropical Southeast Asia, hosts 3 species of Rattus endemic to elevations above 2000 m with an apparent convergence in external morphology: Rattus korinchi and R. hoogerwerfi from Sumatra, and R. baluensis from Borneo. A fourth one, R. tiomanicus, is restricted to lowland elevations across the whole region. The origins of these endemics are little known due to the absence of a robust phylogenetic framework. We use complete mitochondrial genomes from the 3 high altitude Rattus, and several related species to determine their relationships, date divergences, reconstruct their history of colonization, and test for selection on the mitochondrial DNA. We show that mountain colonization happened independently in Borneo (<390 Kya) and Sumatra (~1.38 Mya), likely from lowland lineages. The origin of the Bornean endemic R. baluensis is very recent and its genetic diversity is nested within the diversity of R. tiomanicus. We found weak evidence of positive selection in the high-elevation lineages and attributed the greater nonsynonymous mutations on these branches (specially R. baluensis) to lesser purifying selection having acted on the terminal branches in the phylogeny.

The Genetic Architecture of Plant Defense Trade-offs in a Common Monkeyflower

Abstract: Determining how adaptive combinations of traits arose requires understanding the prevalence and scope of genetic constraints. Frequently observed phenotypic correlations between plant growth, defenses, and/or reproductive timing have led researchers to suggest that pleiotropy or strong genetic linkage between variants affecting independent traits is pervasive. Alternatively, these correlations could arise via independent mutations in different genes for each trait and extensive correlational selection. Here we evaluate these alternatives by conducting a quantitative trait loci (QTL) mapping experiment involving a cross between 2 populations of common monkeyflower (Mimulus guttatus) that differ in growth rate as well as total concentration and arsenal composition of plant defense compounds, phenylpropanoid glycosides (PPGs). We find no evidence that pleiotropy underlies correlations between defense and growth rate. However, there is a strong genetic correlation between levels of total PPGs and flowering time that is largely attributable to a single shared QTL. While this result suggests a role for pleiotropy/close linkage, several other QTLs also contribute to variation in total PPGs. Additionally, divergent PPG arsenals are influenced by a number of smaller-effect QTLs that each underlie variation in 1 or 2 PPGs. This result indicates that chemical defense arsenals can be finely adapted to biotic environments despite sharing a common biochemical precursor. Together, our results show correlations between defense and life-history traits are influenced by pleiotropy or genetic linkage, but genetic constraints may have limited impact on future evolutionary responses, as a substantial proportion of variation in each trait is controlled by independent loci.

Range-Wide Population Structure of 3 Deepwater Eteline Snappers Across the Indo-Pacific Basin.

Abstract: Deep-sea habitats may drive unique dispersal and demographic patterns for fishes, but population genetic analyses to address these questions have rarely been conducted for fishes in these environments. This study investigates the population structure of 3 tropical deepwater snappers of the genus Etelis that reside at 100-400 m depth, with broad and overlapping distributions in the Indo-Pacific. Previous studies showed little population structure within the Hawaiian Archipelago for 2 of these species: Etelis coruscans and E. carbunculus. Here we extend sampling to the entire geographic range of each species to resolve the population genetic architecture for these 2 species, as well as a recently exposed cryptic species (Etelis sp.). One goal was to determine whether deepwater snappers are more dispersive than shallow-water fishes. A second goal was to determine whether submesophotic fishes have older, more stable populations than shallow reef denizens that are subject to glacial sea-level fluctuations. Both goals are pertinent to the management of these valuable food fishes. A total of 1153 specimens of E. coruscans from 15 geographic regions were analyzed, along with 1064 specimens of E. carbunculus from 11 regions, and 590 specimens of E. sp. from 16 regions. The first 2 species were analyzed with mtDNA and 9-11 microsatellite loci, while E. sp. was analyzed with mtDNA only. Etelis coruscans had a non-significant microsatellite global F-ST, but significant global mtDNA Phi(ST) = 0.010 (P = 0.0007), with the isolation of Seychelles in the western Indian Ocean, and intermittent signals of isolation for the Hawaiian Archipelago. Etelis carbunculus had a non-significant microsatellite global F-ST, and significant global mtDNA Phi(ST) = 0.021 (P = 0.0001), with low but significant levels of isolation for Hawai'i, and divergence between Tonga and Fiji. Etelis sp. had mtDNA Phi(ST) = 0.018 (P = 0.0005), with a strong pattern of isolation for both Seychelles and Tonga. Overall, we observed low population structure, shallow mtDNA coalescence (similar to near-shore species), and isolation at the fringes of the Indo-Pacific basin in Hawai'i and the western Indian Ocean. While most shallow-water species have population structure on the scale of biogeographic provinces, deepwater snapper populations are structured on the wider scale of ocean basins, more similar to pelagic fishes than to shallow-water species. This population structure indicates the capacity for widespread dispersal throughout the Indo-Pacific region.

MC1R and KIT Haplotypes Associate With Pigmentation Phenotypes of North American Yak (Bos grunniens).

Abstract: Small numbers of domestic yak (Bos grunniens) were imported to North America in the late 19th century indirectly from the Qinghai-Tibetan Plateau. Coat color of yak is of interest for fiber production, aesthetics, and as a potential indicator of recent hybridization with cattle. North American yak are classified into 3 major coat color patterns depending upon the presence and extent of white markings. They are further classified by nose pigmentation (black or gray). The aim of this study was to identify loci involved in white patterning and nose pigmentation of North American yak. Genotyping by mass spectrometry of markers identified through Sanger and whole-genome sequencing revealed a 388 kb haplotype of KIT associated in a semi-dominant manner with white coloration in this population of yak. This KIT haplotype is similar to both a haplotype found in white-faced Chinese yak and to haplotypes found in cattle but is divergent from other Bos species such as bison, gaur, and banteng. Melanocortin 1 receptor (MC1R) was implicated as a dominant determinant of black nose color with a single haplotype containing 2 missense mutations perfectly associated with the phenotype. The MC1R haplotype associated with black nose pigment is also similar to cattle haplotypes. No cattle studied, however, shared either of the 2 haplotypes associated with color in yak, suggesting these alleles were introgressed into yak before they were imported to North America. These results provide molecular insight into the history of North American yak and information from which breeders can determine possible color outcomes of matings.

Heritability Estimates of Antler and Body Traits in White-Tailed Deer (Odocoileus virginianus) From Genomic-Relatedness Matrices

Abstract: Estimating heritability (h2) is required to predict the response to selection and is useful in species that are managed or farmed using trait information. Estimating h2 in free-ranging populations is challenging due to the need for pedigrees; genomic-relatedness matrices (GRMs) circumvent this need and can be implemented in nearly any system where phenotypic and genome-wide single nucleotide polymorphism (SNP) data are available. We estimated the heritability of five body and three antler traits in a free-ranging population of white-tailed deer (Odocoileus virginianus) on Anticosti Island, Quebec, Canada. We generated classic and robust GRMs from >10,000 SNPs: hind foot length, dressed body mass and peroneus muscle mass had high h2 values of 0.62, 0.44 and 0.55, respectively. Heritability in male-only antler features ranged from 0.07 to 0.33 and had high standard errors. We explored the influence of filtering by minor allele frequency and data completion on h2: GRMs derived from fewer SNPs had reduced h2 estimates and the relatedness coefficients significantly deviated from those generated with more SNPs. As a corollary, we discussed limitations to the application of GRMs in the wild, notably how skewed GRMs, specifically many unrelated individuals, can increase variance around h2 estimates. This is the first study to estimate h2 on a free-ranging population of white-tailed deer and should be informative for breeding designs and management as these traits should respond to selection.

High-Quality SNP Linkage Maps Improved QTL Mapping and Genome Assembly in Populus.

Abstract: With the advances in high-throughput sequencing technologies and the development of new software for extracting single nucleotide polymorphisms (SNPs) across a mapping population, it is possible to construct high-quality genetic maps with thousands of SNPs in outbred forest trees. Two parent-specific linkage maps were constructed with restriction site-associated DNA sequencing data from an F1 hybrid population derived from Populus deltoides and Populus simonii, and applied in QTL mapping and genome assembly. The female P. deltoides map contained 4018 SNPs, which were divided into 19 linkage groups under a wide range of LOD thresholds from 7 to 55. The male P. simonii map showed similar characteristics, consisting of 2097 SNPs, which also belonged to 19 linkage groups under LOD thresholds of 7 to 29. The SNP order of each linkage group was optimal among different ordering results from several available software. Moreover, the linkage maps allowed the detection of 39 QTLs underlying tree height and 47 for diameter at breast height. In addition, the linkage maps improved the anchoring of 689 contigs of P. simonii to chromosomes. The 2 parental genetic maps of Populus are of high quality, especially in terms of SNP data quality, the SNP order within linkage groups, and the perfect match between the number of linkage groups and the karyotype of Populus, as well as the excellent performances in QTL mapping and genome assembly. Both approaches for extracting and ordering SNPs could be applied to other species for constructing high-quality genetic maps.