Interpopulation hybridization results in widespread viability selection across the genome in Tigriopus californicus

<p>Abstract</p> <p>Background</p> <p>Genetic interactions within hybrids influence their overall fitness. Understanding the details of these interactions can improve our understanding of speciation. One experimental approach is to investigate deviations from Mendelian expectations (segregation distortion) in the inheritance of mapped genetic markers. In this study, we used the copepod <it>Tigriopus californicus</it>, a species which exhibits high genetic divergence between populations and a general pattern of reduced fitness in F2 interpopulation hybrids. Previous studies have implicated both nuclear-cytoplasmic and nuclear-nuclear interactions in causing this fitness reduction. We identified and mapped population-diagnostic single nucleotide polymorphisms (SNPs) and used these to examine segregation distortion across the genome within F2 hybrids.</p> <p>Results</p> <p>We generated a linkage map which included 45 newly elucidated SNPs and 8 population-diagnostic microsatellites used in previous studies. The map, the first available for the Copepoda, was estimated to cover 75% of the genome and included markers on all 12 <it>T. californicus </it>chromosomes. We observed little segregation distortion in newly hatched F2 hybrid larvae (fewer than 10% of markers at p < 0.05), but strikingly higher distortion in F2 hybrid adult males (45% of markers at p < 0.05). Hence, segregation distortion was primarily caused by selection against particular genetic combinations which acted between hatching and maturity. Distorted markers were not distributed randomly across the genome but clustered on particular chromosomes. In contrast to other studies in this species we found little evidence for cytonuclear coadaptation. Instead, different linkage groups exhibited markedly different patterns of distortion, which appear to have been influenced by nuclear-nuclear epistatic interactions and may also reflect genetic load carried within the parental lines.</p> <p>Conclusion</p> <p>Adult male F2 hybrids between two populations of <it>T. californius </it>exhibit dramatic segregation distortion across the genome. Distorted loci are clustered within specific linkage groups, and the direction of distortion differs between chromosomes. This segregation distortion is due to selection acting between hatching and adulthood.</p

A gene-based SNP resource and linkage map for the copepod Tigriopus californicus

<p>Abstract</p> <p>Background</p> <p>As yet, few genomic resources have been developed in crustaceans. This lack is particularly evident in Copepoda, given the extraordinary numerical abundance, and taxonomic and ecological diversity of this group. <it>Tigriopus californicus </it>is ideally suited to serve as a genetic model copepod and has been the subject of extensive work in environmental stress and reproductive isolation. Accordingly, we set out to develop a broadly-useful panel of genetic markers and to construct a linkage map dense enough for quantitative trait locus detection in an interval mapping framework for <it>T. californicus--</it>a first for copepods.</p> <p>Results</p> <p>One hundred and ninety Single Nucleotide Polymorphisms (SNPs) were used to genotype our mapping population of 250 F₂larvae. We were able to construct a linkage map with an average intermarker distance of 1.8 cM, and a maximum intermarker distance of 10.3 cM. All markers were assembled into linkage groups, and the 12 linkage groups corresponded to the 12 known chromosomes of <it>T. californicus</it>. We estimate a total genome size of 401.0 cM, and a total coverage of 73.7%. Seventy five percent of the mapped markers were detected in 9 additional populations of <it>T. californicus</it>. Of available model arthropod genomes, we were able to show more colocalized pairs of homologues between <it>T. californicus </it>and the honeybee <it>Apis mellifera</it>, than expected by chance, suggesting preserved macrosynteny between Hymenoptera and Copepoda.</p> <p>Conclusions</p> <p>Our study provides an abundance of linked markers spanning all chromosomes. Many of these markers are also found in multiple populations of <it>T. californicus</it>, and in two other species in the genus. The genomic resource we have developed will enable mapping throughout the geographical range of this species and in closely related species. This linkage map will facilitate genome sequencing, mapping and assembly in an ecologically and taxonomically interesting group for which genomic resources are currently under development.</p

Genomic signatures of mitonuclear coevolution across populations of Tigriopus californicus

The copepod Tigriopus californicus shows extensive population divergence and is becoming a model for understanding allopatric differentiation and the early stages of speciation. Here, we report a high-quality reference genome for one population (similar to 190 megabases across 12 scaffolds, and similar to 15,500 protein-coding genes). Comparison with other arthropods reveals 2,526 genes presumed to be specific to T. californicus, with an apparent proliferation of genes involved in ion transport and receptor activity. Beyond the reference population, we report re-sequenced genomes of seven additional populations, spanning the continuum of reproductive isolation. Populations show extreme mitochondrial DNA divergence, with higher levels of amino acid differentiation than observed in other taxa. Across the nuclear genome, we find elevated protein evolutionary rates and positive selection in genes predicted to interact with mitochondrial DNA and the proteins and RNA it encodes in multiple pathways. Together, these results support the hypothesis that rapid mitochondrial evolution drives compensatory nuclear evolution within isolated populations, thereby providing a potentially important mechanism for causing intrinsic reproductive isolation

Redescription of *Aulactinia veratra* n.comb. (=*Cnidopus veratra*) (Coelenterata: Actiniaria) from Australia

Asterisks (*...*) surround words or phrases that are to be italicized.The actinian described as *Actinia veratra* Drayton, 1846, and currently referred to as *Cnidopus veratra*, belongs to the genus *Aulactinia*. Discrepancies in the literature, particularly concerning ectodermal specializations of the column, led to taxonomic uncertainties about its placement. Nomenclatural re-evaluation was necessitated by recent synonymization of the genus *Cnidopus* with *Epiactis*. *Cribrina verruculata* Lager, 1911, is synonymized with *Aulactinia veratra*

Data from: The genomic trajectory of hybrid swarms: outcomes of repeated crosses between populations of Tigriopus californicus

Introgressive hybridization between genetically divergent populations is an important evolutionary process. The degree to which repeated hybridization events between the same parental taxa lead to similar genomic outcomes is unknown. This study addressed this question by following genomic trajectories of replicate hybrid swarms of the copepod Tigriopus californicus over many generations of free mating. Swarm composition was determined both by differential reproductive success of founder individuals and subsequent selection on hybrid genotypes. For one cross, between two populations showing differential fitness in the laboratory and no hybrid breakdown, the genetic trajectory was highly repeatable: replicates rapidly became dominated by alleles from the fitter parent. In a second cross, between two populations showing similar fitness and significant F2 hybrid breakdown, alleles from alternative populations dominated different replicates. Swarms exhibited a general temporal trend of decreasing cytonuclear mismatch. Some patterns of differential introgression across the genome were strikingly congruent amongst swarm replicates, both within and between cross types, and reflected patterns of segregation distortion previously observed within controlled crosses between the same parental populations. Differences in heterozygosity between the sexes, and evidence for a previously suspected sex-distortion locus, suggest that complex interactions between sex and genotype influence hybrid swarm outcome

Data from: Recovery from hybrid breakdown in a marine invertebrate is faster, stronger and more repeatable under environmental stress

Understanding how environmental stress alters the consequences of hybridization is important, because the rate of hybridization and the likelihood of hybrid speciation both appear elevated in harsh, disturbed or marginal habitats. We assessed fitness, morphometrics and molecular genetic composition over 14 generations of hybridization between two highly divergent populations of the marine copepod Tigriopus californicus. Replicated, experimental hybrid populations in both control and high salinity conditions showed a decline in fitness, followed by a recovery. Recovery was faster in the salinity stress treatment, returning to parental levels up to two generations earlier than in the control. This recovery was stable in the high salinity treatment, while in the control treatment fitness dropped back below parental levels at the final time point. Recovery in the high salinity treatment was also stronger in terms of competitive fitness and heat shock tolerance. Finally, consequences of hybridization were more repeatable under salinity stress, where among-replicate variance for survivorship and molecular genetic composition was lower than in the control treatment. In a system with low effective population sizes (estimates ranged from 17 to 63), where genetic drift might be expected to be the predominate force, strong selection under harsh environmental conditions apparently promoted faster, stronger and more repeatable recovery from depressed hybrid fitness

t_californicus_rqtl_file

File used for rqtl, including marker linkage data, individual marker data (allele by population of origin, or heterozygote), phenotypic data (measured in the lab), mitochondrial background and sex

t_californicus_raw_morphodata

This contains the raw developmental and morphological data, as well as the transformed and mean-corrected value

SNP calls for all T. californicus individuals genotyped.

SNP genotypes for all T. californicus individuals analyzed in the associated study. Genotyping was performed using iPLEX Gold on a MassARRAY Compact (Sequenom). SNPs (prefix TC) are arranged in map order by linkage group (12 chromosomes plus mitochondrion). 'Month 0' indicates individuals collected from pure founder populations immediately prior to the establishment of experimental swarms. Abbreviations are: f: female; m: male; na: not applicable; nc: no call, an unambiguous genotype was not obtained for this individual at this SNP

Fitness data

Data on hatching, survival and metamorphosis across 13 generation