Threespine Stickleback Fish Research Articles

Enhanced ambient UVB radiation affects post-mating, but not pre-mating sexual traits in a fish.

Organisms inhabiting shallow aquatic habitats currently experience increasing levels of solar ultraviolet B radiation (UVB). UVB causes damage on cellular and molecular levels and can affect associated life-history traits either through direct exposure or indirectly through oxidative stress generation. We examined UVB effects on pre- and post-mating sexual traits in three-spined stickleback fish (Gasterosteus aculeatus). Adult, reproductively non-active males were assigned to two exposure treatments under semi-natural conditions in an outdoor experiment; one group received natural radiation (UVBnormal) whilst the other group received additional UVB (UVBenhanced). After two months, colour metrics were used to quantify male breeding colouration as pre-mating trait. At the post-mating stage, sperm morphology, number and movement as well as testes mass were determined. Males did not significantly differ in sexual ornamentation between treatments, but UVBenhanced fish had smaller testes as well as fewer and shorter sperm than UVBnormal fish. Sperm movement was not significantly different between treatments. However, in UVBenhanced males, linear and progressive movement of sperm was positively correlated with sperm morphology (head-to-tail length ratio), whereas in UVBnormal males this relationship was negative (but not significant). Additionally, there was a significant treatment by body condition interaction concerning head-to-tail length ratio, i.e. head-to-tail length ratio increased with condition in UVBnormal males whereas there was no relationship in UVBenhanced fish. Our findings reveal that increased UVB levels influence post-mating fitness-relevant traits in males whilst having no significant impact on pre-mating sexual traits, suggesting selectiveUVB-effects at the gamete level with consequences for reproductive performance.

Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks.

Regulation of gene expression is thought to play a major role in adaptation, but the relative importance of cis- and trans- regulatory mechanisms in the early stages of adaptive divergence is unclear. Using RNAseq of threespine stickleback fish gill tissue from four independent marine-freshwater ecotype pairs and their F1 hybrids, we show that cis-acting (allele-specific) regulation consistently predominates gene expression divergence. Genes showing parallel marine-freshwater expression divergence are found near to adaptive genomic regions, show signatures of natural selection around their transcription start sites and are enriched for cis-regulatory control. For genes with parallel increased expression among freshwater fish, the quantitative degree of cis- and trans-regulation is also highly correlated across populations, suggesting a shared genetic basis. Compared to other forms of regulation, cis-regulation tends to show greater additivity and stability across different genetic and environmental contexts, making it a fertile substrate for the early stages of adaptive evolution.

Advancing threespine stickleback as an outbred immunogenetics model by pinpointing the onset of adaptive immunity

Abstract The development of an outbred immunogenetics model system is needed to understand how genetic variation impacts phenotypic variation of disease states in humans. Threespine stickleback fish (Gasterosteus aculeatus) provide just such a model. Stickleback are genetically tractable laboratory organisms with a well-annotated genome, but with lines drawn from populations inhabiting vastly different habitats. Individuals from different populations show high levels of genetic variation. The onset of the adaptive immune system is currently unknown in stickleback, a significant hindrance in studies of immunodeficiency diseases. To characterize the early development of adaptive immunity, we will analyze the expression of known early indicators of adaptive immunity maturation. These include recombination activating genes, rag1 and rag2, which are essential to the maturation of T and B lymphocytes, and T cell receptor genes, tcr-β and tcr-γ, which are expressed in mature T lymphocytes. To analyze the expression of rag1, rag2, tcr-β, and tcr-γ, we will perform whole mount in situ hybridization throughout a developmental time series to detect when and where the genes are first expressed, with special focus on the head kidney and the thymus, followed by qPCR to quantify the expression of the early adaptive immunity genes. Knowing when adaptive immunity onset occurs in threespine stickleback advances threespine stickleback as an outbred disease model in immunogenetics studies, allowing manipulative studies of immunological disease phenotypes in the context of genetic variation.

Development of an outbred disease model of Hermansky-Pudlak Syndrome in Threespine Stickleback

Abstract Mounting evidence shows that humans respond heterogeneously to diseases and treatments due to their genetic variation, leading to the growth of the field of personalized medicine. Research on model organisms is vital to seek scientific understandings of disease in this broader context, but current research in nonhuman disease models struggles to demonstrate the genetic variability of humans. One disease that exemplifies this issue is Hermansky-Pudlak Syndrome (HPS). HPS is a genetic syndrome resulting from mutations in one of ten HPS genes involved in endosome trafficking, which can result in oculocutaneous albinism, blood diathesis, pulmonary fibrosis, vision impairment, and granulomatous enterocolitis phenotypically indistinguishable from Crohn’s Disease. Currently no disease models for HPS exist that accurately demonstrate the variability of the human disease. Here we present an outbred mutant model of threespine stickleback (Gasterosteus aculeatus) fish exhibiting symptoms consistent with HPS. Using genetic mapping approaches we narrowed this mutation to a region of the genome containing hps4the causative disease gene of Hermansky-Pudlak Syndrome Type 4. Using histological staining and imaging we are confirming the presence of each symptom comprising the syndrome and hope to develop the first outbred system to tackle this disease. Ultimately, the application of outbred medical models in diverse organisms will be important for the advancement of personalized medicine, greatly enhancing our understanding of how genetic variation affects disease states.

Divergent Fine-Scale Recombination Landscapes between a Freshwater and Marine Population of Threespine Stickleback Fish.

Meiotic recombination is a highly conserved process that has profound effects on genome evolution. At a fine-scale, recombination rates can vary drastically across genomes, often localized into small recombination “hotspots” with highly elevated rates, surrounded by regions with little recombination. In most species studied, the location of hotspots within genomes is highly conserved across broad evolutionary timescales. The main exception to this pattern is in mammals, where hotspot location can evolve rapidly among closely related species and even among populations within a species. Hotspot position in mammals is controlled by the gene, Prdm9, whereas in species with conserved hotspots, a functional Prdm9 is typically absent. Due to a limited number of species where recombination rates have been estimated at a fine-scale, it remains unclear whether hotspot conservation is always associated with the absence of a functional Prdm9. Threespine stickleback fish (Gasterosteus aculeatus) are an excellent model to examine the evolution of recombination over short evolutionary timescales. Using a linkage disequilibrium-based approach, we found recombination rates indeed varied at a fine-scale across the genome, with many regions organized into narrow hotspots. Hotspots had highly divergent landscapes between stickleback populations, where only ∼15% of these hotspots were shared. Our results indicate that fine-scale recombination rates may be diverging between closely related populations of threespine stickleback fish. Interestingly, we found only a weak association of a PRDM9 binding motif within hotspots, which suggests that threespine stickleback fish may possess a novel mechanism for targeting recombination hotspots at a fine-scale.

Genome Characterization, Prevalence, and Transmission Mode of a Novel Picornavirus Associated with the Threespine Stickleback Fish (Gasterosteus aculeatus).

The complete genome sequence of an RNA virus was assembled from RNA sequencing of virus particles purified from threespine stickleback intestine tissue samples. This new virus is most closely related to the Eel picornavirus and can be assigned to the genus Potamipivirus in the family Picornaviridae Its unique genetic properties are enough to establish a new species, dubbed the Threespine Stickleback picornavirus (TSPV). Due to their broad geographic distribution throughout the Northern Hemisphere and parallel adaptation to freshwater, threespine sticklebacks have become a model in evolutionary ecology. Further analysis using diagnostic PCRs revealed that TSPV is highly prevalent in both anadromous and freshwater populations of threespine sticklebacks, infects almost all fish tissues, and is transmitted vertically to offspring obtained from in vitro fertilization in laboratory settings. Finally, TSPV was found in Sequence Reads Archives of transcriptome of Gasterosteus aculeatus, further demonstrating its wide distribution and unsought prevalence in samples. It is thus necessary to test the impact of TSPV on the biology of threespine sticklebacks, as this widespread virus could interfere with the behavioral, physiological, or immunological studies that employ this fish as a model system.IMPORTANCE The threespine stickleback species complex is an important model system in ecological and evolutionary studies because of the large number of isolated divergent populations that are experimentally tractable. For similar reasons, its coevolution with the cestode parasite Schistocephalus solidus, its interaction with gut microbes, and the evolution of its immune system are of growing interest. Herein we describe the discovery of an RNA virus that infects both freshwater and anadromous populations of sticklebacks. We show that the virus is transmitted vertically in laboratory settings and found it in Sequence Reads Archives, suggesting that experiments using sticklebacks were conducted in the presence of the virus. This discovery can serve as a reminder that the presence of viruses in wild-caught animals is possible, even when animals appear healthy. Regarding threespine sticklebacks, the impact of Threespine Stickleback picornavirus (TSPV) on the fish biology should be investigated further to ensure that it does not interfere with experimental results.

Consequences of divergent temperature optima in a host–parasite system

It was suggested that parasite infections become more severe with rising temperature, as expected during global warming. In ectothermic systems, the growth of a parasite and therefore its reproductive capacity is expected to increase with temperature. However, the outcome of the interaction depends on the temperature optima of both host and parasite. Here we used experimental infections of three‐spined stickleback fish Gasterosteus aculeatus with its specific tapeworm parasite Schistocephalus solidus to investigate in detail the temperature optima for both host and parasite. We analyzed the fitness consequences thereof, focusing on growth and immunity of the host, and growth and offspring production of the parasite as fitness correlates. We checked for potential differences among populations, using the offspring of hosts and parasites derived from four study sites in Iceland, Germany and Spain that differ in average annual temperature ranging between 4.8°C and 18.4°C. We found differences in temperature optima of host and parasites that were quite consistent across the populations: while sticklebacks grew faster and had higher immune activity at low temperatures, the parasites did not even grow fast enough to reach sexual maturity in these conditions. By contrast, with increasing temperatures, parasite growth, egg production and offspring hatching increased strongly while host immunity and growth were impaired. Our results show that divergent temperature optima of hosts and parasites can have drastic fitness consequences and support the expectation that some parasites will benefit from global warming.

Predictable genome-wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish.

Genomic studies of parallel (or convergent) evolution often compare multiple populations diverged into two ecologically different habitats to search for loci repeatedly involved in adaptation. Because the shared ancestor of these populations is generally unavailable, the source of the alleles at adaptation loci, and the direction in which their frequencies were shifted during evolution, remain elusive. To shed light on these issues, we here use multiple populations of threespine stickleback fish adapted to two different types of derived freshwater habitats—basic and acidic lakes on the island of North Uist, Outer Hebrides, Scotland—and the present‐day proxy of their marine ancestor. In a first step, we combine genome‐wide pooled sequencing and targeted individual‐level sequencing to demonstrate that ecological and phenotypic parallelism in basic‐acidic divergence is reflected by genomic parallelism in dozens of genome regions. Exploiting data from the ancestor, we next show that the acidic populations, residing in ecologically more extreme derived habitats, have adapted by accumulating alleles rare in the ancestor, whereas the basic populations have retained alleles common in the ancestor. Genomic responses to selection are thus predictable from the ecological difference of each derived habitat type from the ancestral one. This asymmetric sorting of standing genetic variation at loci important to basic‐acidic divergence has further resulted in more numerous selective sweeps in the acidic populations. Finally, our data suggest that the maintenance in marine fish of standing variation important to adaptive basic‐acidic differentiation does not require extensive hybridization between the marine and freshwater populations. Overall, our study reveals striking genome‐wide determinism in both the loci involved in parallel divergence, and in the direction in which alleles at these loci have been selected.

A Single Interacting Species Leads to Widespread Parallel Evolution of the Stickleback Genome

Biotic interactions are potent, widespread causes of natural selection and divergent phenotypic evolution and can lead to genetic differentiation with gene flow among wild populations ("isolation by ecology") [1-4]. Biotic selection has been predicted to act onmore genes than abiotic selection thereby drivinggreater adaptation [5]. However, difficulties in isolating the genome-wide effect of single biotic agents of selection have limited our ability to identify and quantify the number and type of genetic regions responding to biotic selection [6-9]. We identified geographically interspersed lakes in which threespine stickleback fish (Gasterosteus aculeatus) have repeatedly adapted to the presence or absence of a single member of the ecological community, prickly sculpin (Cottus asper), a fish that is both a competitor and a predator of the stickleback [10]. Whole-genome sequencing revealed that sculpin presence or absence accounted for the majority of genetic divergence among stickleback populations, more so than geography. The major axis of genomic variation within and between the two lake types was correlated with multiple traits, indicating parallel natural selection across a gradient of biotic environments. A large proportion of the genome-about 1.8%, encompassing more than 600 genes-differentiated stickleback from the two biotic environments. Divergence occurred in 141 discrete genomic clumps located mainly in regions of low recombination, suggesting that genes brought to lakes by the colonizing ancestral population often evolved together in linked blocks. Strong selection and a wealth of standing genetic variation explain how a single member of the biotic community can have such a rapid and profound evolutionary impact.

Replicated evolutionary inhibition of a complex ancestral behaviour in an adaptive radiation.

Adaptive radiations often exhibit high levels of phenotypic replication, a phenomenon that can be explained by selection on standing variation in repeatedly divergent environments or by the influence of ancestral plasticity on selection in divergent environments. Here, we offer the first evidence that plastic loss of expression of a complex display in a novel environment, followed by selection against expression, could lead to replicated evolutionary inhibition of the phenotype. In both ancestral (oceanic) and benthic (freshwater) populations of the threespine stickleback fish, cannibalism is common and males defending nests respond to approaching groups with a complex diversionary display. This display is not exhibited by males in allopatric, limnetic (freshwater) populations from which cannibalistic groups are absent. Laboratory-reared males from three limnetic populations exhibit a reduced tendency to respond to cannibalistic foraging groups relative to laboratory-reared ancestral and benthic males, but still are capable of producing a similar array of forms of the display despite many generations of disuse. Thus, replication in adaptive radiations can reflect reduced expression of an ancestral trait followed by evolutionary inhibition while the population retains the capacity to express the trait under extreme ancestral conditions.

Parallel transcriptome evolution in stream threespine sticklebacks.

Natural selection can cause similar phenotypic evolution in phylogenetically independent lineages inhabiting similar environments. Compared to morphological, behavioral, and physiological traits, little is known about the parallel evolution of transcriptome. Furthermore, the relative contribution of cis- and trans-regulatory changes to parallel transcriptome evolution largely remains unclear. The threespine stickleback fish (Gasterosteus aculeatus) is a great model for studying parallel evolution because its ancestral marine populations independently colonized freshwater habitats in multiple geographical regions, resulting in independent pairs of marine and freshwater ecotypes in each region. Here, we investigated transcriptomic parallelism among the marine and stream ecotypes of Japanese and Canadian threespine sticklebacks by conducting common garden experiments and microarray analysis of the brain, which controls several physiological and behavioral traits differing between these ecotypes. We found parallel expression differences in 103 genes, including those encoding the enzymes involved in taurine synthesis and glycoprotein hydrolysis. The number of genes differentially expressed in parallel was significantly larger than the number of genes showing an antiparallel pattern (71 genes). To investigate the genetic architecture underlying transcriptome divergence, we re-analyzed the previous expression quantitative trait locus (eQTL) data and found that most eQTLs were located on the same chromosome as the transcripts, possibly in cis-regulatory regions. Furthermore, the effect sizes of the eQTLs on the same chromosomes were larger than those on different chromosomes. Thus, we found that divergence in the brain transcriptome between the ecotypes shows parallelism and is mainly caused by genetic changes occurring on the same chromosome as the target genes.

Evolution of steroid hormones in reproductive females of the threespine stickleback fish

Hormones play a prominent role in animal development, mediating the expression of traits and coordinating phenotypic responses to the environment. Their role as physiological integrators has implications for how populations respond to natural selection and can impact the speed and direction of evolutionary change. However, many emerging and established fish models with the potential to be ecologically or evolutionarily informative are small-bodied, making hormone sampling through traditional methods (whole-body or plasma) lethal or highly disruptive. Sampling methodology has thus restricted study design, often limiting sample sizes, and has prevented the study of at-risk/endangered populations. We utilize water-borne hormone sampling, a minimally invasive method of measuring the rate of steroid hormone release across the gills and further validate this method in a novel, evolutionary context. First, we compare water-borne hormone measures of cortisol with those quantified from plasma and whole-body samples collected from the same individuals to establish the relationship between concentrations quantified via the three methods. We then compare the release of steroid hormones in three populations of threespine stickleback to establish the sensitivity of this tool in measuring within-individual and between-individual variation in biologically relevant contexts (reproductive stages), and in assessing differences among populations with distinct evolutionary histories. We demonstrate a strong positive relationship between cortisol concentrations measured with water-borne, plasma, and whole-body collection techniques. Tracking estradiol and testosterone throughout clutch production in females produced anticipated patterns associated with growing and maturing eggs, with divergence in estradiol production in one population. Additionally, differences among populations in cortisol levels at ovulation paralleled the relative presence of a social stressor, and thus expected energetic needs within each population. We confirm that water-borne hormone sampling is sufficiently sensitive to capture biologically relevant fluctuations in steroid hormones between environmental contexts and demonstrate that among-population differences are detectable. This technique can be applied broadly to small fish to answer important ecological and evolutionary questions. By linking population variation in hormones and the multivariate phenotype, this technique will help elucidate both proximate mechanisms underlying phenotypic development and variation, and the way hormone networks alter evolutionary responses to selection.

An intronic enhancer of Bmp6 underlies evolved tooth gain in sticklebacks.

Threespine stickleback fish offer a powerful system to dissect the genetic basis of morphological evolution in nature. Marine sticklebacks have repeatedly invaded and adapted to numerous freshwater environments throughout the Northern hemisphere. In response to new diets in freshwater habitats, changes in craniofacial morphology, including heritable increases in tooth number, have evolved in derived freshwater populations. Using a combination of quantitative genetics and genome resequencing, here we fine-mapped a quantitative trait locus (QTL) regulating evolved tooth gain to a cluster of ten QTL-associated single nucleotide variants, all within intron four of Bone Morphogenetic Protein 6 (Bmp6). Transgenic reporter assays revealed this intronic region contains a tooth enhancer. We induced mutations in Bmp6, revealing required roles for survival, growth, and tooth patterning. Transcriptional profiling of Bmp6 mutant dental tissues identified significant downregulation of a set of genes whose orthologs were previously shown to be expressed in quiescent mouse hair stem cells. Collectively these data support a model where mutations within a Bmp6 intronic tooth enhancer contribute to evolved tooth gain, and suggest that ancient shared genetic circuitry regulates the regeneration of diverse vertebrate epithelial appendages including mammalian hair and fish teeth.

Convergent evolution of gene expression in two high-toothed stickleback populations.

Changes in developmental gene regulatory networks enable evolved changes in morphology. These changes can be in cis regulatory elements that act in an allele-specific manner, or changes to the overall trans regulatory environment that interacts with cis regulatory sequences. Here we address several questions about the evolution of gene expression accompanying a convergently evolved constructive morphological trait, increases in tooth number in two independently derived freshwater populations of threespine stickleback fish (Gasterosteus aculeatus). Are convergently evolved cis and/or trans changes in gene expression associated with convergently evolved morphological evolution? Do cis or trans regulatory changes contribute more to gene expression changes accompanying an evolved morphological gain trait? Transcriptome data from dental tissue of ancestral low-toothed and two independently derived high-toothed stickleback populations revealed significantly shared gene expression changes that have convergently evolved in the two high-toothed populations. Comparing cis and trans regulatory changes using phased gene expression data from F1 hybrids, we found that trans regulatory changes were predominant and more likely to be shared among both high-toothed populations. In contrast, while cis regulatory changes have evolved in both high-toothed populations, overall these changes were distinct and not shared among high-toothed populations. Together these data suggest that a convergently evolved trait can occur through genetically distinct regulatory changes that converge on similar trans regulatory environments.

Repeated Selection of Alternatively Adapted Haplotypes Creates Sweeping Genomic Remodeling in Stickleback.

Heterogeneous genetic divergence can accumulate across the genome when populations adapt to different habitats while still exchanging alleles. How long does diversification take and how much of the genome is affected? When divergence occurs in parallel from standing genetic variation, how often are the same haplotypes involved? We explore these questions using restriction site-associated DNA sequencing genotyping data and show that broad-scale genomic repatterning, fueled by copious standing variation, can emerge in just dozens of generations in replicate natural populations of threespine stickleback fish (Gasterosteus aculeatus). After the catastrophic 1964 Alaskan earthquake, marine stickleback colonized newly created ponds on seismically uplifted islands. We find that freshwater fish in these young ponds differ from their marine ancestors across the same genomic segments previously shown to have diverged in much older lake populations. Outside of these core divergent regions the genome shows no population structure across the ocean-freshwater divide, consistent with strong local selection acting in alternative environments on stickleback populations still connected by significant gene flow. Reinforcing this inference, a majority of divergent haplotypes that are at high frequency in ponds are detectable in the sea, even across great geographic distances. Building upon previous population genomics work in this model species, our data suggest that a long history of divergent selection and gene flow among stickleback populations in oceanic and freshwater habitats has maintained polymorphisms of alternatively adapted DNA sequences that facilitate parallel evolution.

Genetic Dissection of a Supergene Implicates Tfap2a in Craniofacial Evolution of Threespine Sticklebacks.

In nature, multiple adaptive phenotypes often coevolve and can be controlled by tightly linked genetic loci known as supergenes. Dissecting the genetic basis of these linked phenotypes is a major challenge in evolutionary genetics. Multiple freshwater populations of threespine stickleback fish (Gasterosteus aculeatus) have convergently evolved two constructive craniofacial traits, longer branchial bones and increased pharyngeal tooth number, likely as adaptations to dietary differences between marine and freshwater environments. Prior QTL mapping showed that both traits are partially controlled by overlapping genomic regions on chromosome 21 and that a regulatory change in Bmp6 likely underlies the tooth number QTL. Here, we mapped the branchial bone length QTL to a 155 kb, eight-gene interval tightly linked to, but excluding the coding regions of Bmp6 and containing the candidate gene Tfap2a Further recombinant mapping revealed this bone length QTL is separable into at least two loci. During embryonic and larval development, Tfap2a was expressed in the branchial bone primordia, where allele specific expression assays revealed the freshwater allele of Tfap2a was expressed at lower levels relative to the marine allele in hybrid fish. Induced loss-of-function mutations in Tfap2a revealed an essential role in stickleback craniofacial development and show that bone length is sensitive to Tfap2a dosage in heterozygotes. Combined, these results suggest that closely linked but genetically separable changes in Bmp6 and Tfap2a contribute to a supergene underlying evolved skeletal gain in multiple freshwater stickleback populations.

Ancient genomic variation underlies repeated ecological adaptation in young stickleback populations.

Adaptation in the wild often involves standing genetic variation (SGV), which allows rapid responses to selection on ecological timescales. However, we still know little about how the evolutionary histories and genomic distributions of SGV influence local adaptation in natural populations. Here, we address this knowledge gap using the threespine stickleback fish (Gasterosteus aculeatus) as a model. We extend restriction site‐associated DNA sequencing (RAD‐seq) to produce phased haplotypes approaching 700 base pairs (bp) in length at each of over 50,000 loci across the stickleback genome. Parallel adaptation in two geographically isolated freshwater pond populations consistently involved fixation of haplotypes that are identical‐by‐descent. In these same genomic regions, sequence divergence between marine and freshwater stickleback, as measured by dXY, reaches tenfold higher than background levels and genomic variation is structured into distinct marine and freshwater haplogroups. By combining this dataset with a de novo genome assembly of a related species, the ninespine stickleback (Pungitius pungitius), we find that this habitat‐associated divergent variation averages six million years old, nearly twice the genome‐wide average. The genomic variation that is involved in recent and rapid local adaptation in stickleback has therefore been evolving throughout the 15‐million‐year history since the two species lineages split. This long history of genomic divergence has maintained large genomic regions of ancient ancestry that include multiple chromosomal inversions and extensive linked variation. These discoveries of ancient genetic variation spread broadly across the genome in stickleback demonstrate how selection on ecological timescales is a result of genome evolution over geological timescales, and vice versa.

Brain differences in ecologically differentiated sticklebacks.

Populations that have recently diverged offer a powerful model for studying evolution. Ecological differences are expected to generate divergent selection on multiple traits, including neurobiological ones. Animals must detect, process, and act on information from their surroundings and the form of this information can be highly dependent on the environment. We might expect different environments to generate divergent selection not only on the sensory organs, but also on the brain regions responsible for processing sensory information. Here, we test this hypothesis using recently evolved reproductively isolated species pairs of threespine stickleback fish Gasterosteus aculeatus that have well-described differences in many morphological and behavioral traits correlating with ecological differences. We use a state-of-the-art method, magnetic resonance imaging, to get accurate volumetric data for 2 sensory processing regions, the olfactory bulbs and optic tecta. We found a tight correlation between ecology and the size of these brain regions relative to total brain size in 2 lakes with intact species pairs. Limnetic fish, which rely heavily on vision, had relatively larger optic tecta and smaller olfactory bulbs compared with benthic fish, which utilize olfaction to a greater extent. Benthic fish also had larger total brain volumes relative to their body size compared with limnetic fish. These differences were erased in a collapsed species pair in Enos Lake where anthropogenic disturbance has led to intense hybridization. Together these data indicate that evolution of sensory processing regions can occur rapidly and independently.

Changes in behavior and brain immediate early gene expression in male threespined sticklebacks as they become fathers

Motherhood is a period of intense behavioral and brain activity. However, we know less about the neural and molecular mechanisms associated with the demands of fatherhood. Here, we report the results of two experiments designed to track changes in behavior and brain activation associated with fatherhood in male threespined stickleback fish (Gasterosteus aculeatus), a species in which fathers are the sole providers of parental care. In experiment 1, we tested whether males' behavioral reactions to different social stimuli depends on parental status, i.e. whether they were providing parental care. Parental males visited their nest more in response to social stimuli compared to nonparental males. Rates of courtship behavior were high in non-parental males but low in parental males. In experiment 2, we used a quantitative in situ hybridization method to compare the expression of an immediate early gene (Egr-1) across the breeding cycle – from establishing a territory to caring for offspring. Egr-1 expression peaked when the activities associated with fatherhood were greatest (when they were providing care to fry), and then returned to baseline levels once offspring were independent. The medial dorsal telencephalon (basolateral amygdala), lateral part of dorsal telencephalon (hippocampus) and anterior tuberal nucleus (ventral medial hypothalamus) exhibited high levels of Egr-1 expression during the breeding cycle. These results help to define the neural circuitry associated with fatherhood in fishes, and are consistent with the hypothesis that fatherhood – like motherhood – is a period of intense behavioral and neural activity.

Adaptation despite gene flow? Low recombination helps.

About 15,000years earlier, the Northern half of Europe and North America was buried under a few kilometres of ice. Since then, many organisms have colonized and rapidly adapted to the new, vacant habitats. Some, like the threespine stickleback fish, have done so more successfully than others: from the sea, stickleback have adapted to a multitude of lake and stream habitats with a vast array of complex phenotypes and life histories. Previous studies showed that most of these "ecotypes" differ in multiple divergently selected genes throughout the genome. But how are well-adapted ecotypes of one habitat protected from maladaptive gene flow from ecotypes of another, adjacent habitat? According to a From the Cover meta-analysis in this issue of Molecular Ecology (Samuk etal., 2017), low recombination rate regions in the genome offer such protection. While inversions have often been highlighted as an efficient way to maintain linkage disequilibrium among sets of adaptive variants in the face of gene flow, Samuk etal. (2017) show that variation in recombination rate across the genome may perform a similar role in threespine stickleback. With this study, theoretical predictions for the importance of low recombination regions in adaptation are for the first time tested with a highly replicated population genomic data set. The findings from this study have implications for the adaptability of species, speciation and the evolution of genome architecture.