Biology subjects

Martin, C. H.

Publications and source records attributed to Martin, C. H..

5 recordsLinked to original sources

bioRxiv2018

Rampant hybrid misexpression in craniofacial tissues within a recent adaptive radiation of Cyprinodon pupfishes

Genetic incompatibilities constitute the final stages of reproductive isolation and speciation, but little is known about incompatibilities that occur within recent adaptive radiations among closely related diverging populations. Crossing divergent species to form hybrids can break up coadapted variation, resulting in genetic incompatibilities within developmental networks shaping adaptive traits. We crossed two closely related sympatric Cyprinodon pupfish species - a dietary generalist and a specialized molluscivore - and measured expression levels in their F1 hybrids to identify regulatory variation underlying the novel craniofacial morphology found in this recent microendemic adaptive radiation. We extracted mRNA from eight day old whole-larvae tissue and from craniofacial tissues dissected from 17-20 day old larvae to compare gene expression between a total of seven F1 hybrids and 24 individuals from parental species populations. We found 3.9% of genes differentially expressed between generalists and molluscivores in whole-larvae tissues and 0.6% of genes differentially expressed in craniofacial tissue. We found that 2.1% of genes were misexpressed in whole-larvae hybrids at 8 dpf whereas 19.1% of genes were misexpressed in hybrid craniofacial tissue at 17-20 dpf, after correcting for sequencing biases. We also measured allele specific expression across 15,429 phased heterozygous sites to identify regulatory mechanisms underlying differential expression between generalists and molluscivores. Together, our results highlight the importance of considering misexpression as an early indicator of genetic incompatibilities in the context of rapidly diverged morphology and suggests that wide-spread compensatory regulatory divergence drives hybrid misexpression in developing tissues that give rise to novel craniofacial traits.

evolutionary biology↗

bioRxiv2018

Testing the behavioral origins of novelty: did increased aggression lead to scale-eating in pupfishes?

How novelty evolves is still largely unknown. Environmental changes are often assumed to precede novelty; however, behavioral shifts may also play a role. Here, we examine whether a shift in aggression explains the origin of a novel scale-eating pupfish species (Cyprinodon desquamator) within an adaptive radiation on San Salvador Island, Bahamas. We compared aggression using behavioral and gene expression data across three sympatric species in the San Salvador radiation (generalist, snail-eating specialist, and scale-eating specialist), and additionally measured behavioral aggression in an outgroup generalist from North Carolina. Surprisingly, we found increased behavioral aggression and differential expression of aggression-related genes in both the scale-eating and snail-eating species. Furthermore, male scale-eaters and female snail-eaters showed the highest levels of aggression compared to other groups. Differential gene expression in each specialist during larval development also suggested sex-mediated differences in male-male aggression and maternal care. Ultimately, our data indicate that aggression is not unique to scale-eating specialists. Instead, selection may increase aggression in other contexts such as niche specialization, mate competition, or selection on other ecologically relevant traits, including jaw size. Indeed, some adaptive variants associated with oral jaw size in the San Salvador radiation occur in genetic pathways with pleiotropic effects on aggression.

evolutionary biology↗

bioRxiv2017

Oxford Nanopore sequencing in a research-based undergraduate course

BackgroundNanopore sequencing is a third generation genomic sequencing method that offers real time sequencing of DNA samples. Nanopore sequencing is an excellent tool for teaching because it involves cutting-edge sequencing methods and also helps students to develop a research mindset, where students can learn to identify and resolve problems that arise during an experiment.\n\nResultsWe, as a group of undergraduate biology students, were able to use nanopore sequencing to analyze a sample of pupfish DNA. We were able to accomplish this without computer science backgrounds and only some basic DNA extraction training. Although there were issues, such as inconsistent results across runs, we found it useful as a research learning experience and an application of the skills we learned.\n\nConclusionsAs students, it was exciting to be able to experience this technology first hand and apply what we learned in the classroom. Nanopore sequencing holds potential for DNA sequencing of large fragments in real time. It allows students to be acquainted with novel technologies and the theories behind them. However, as with all new techniques, it does not have the same established support, and when students run into difficulties while using nanopore sequencing, it is often difficult to identify what went wrong.

genomics↗

bioRxiv2017

Unique genetic variants underlie parallel gene expression within a young adaptive radiation despite specialization on highly divergent resources

Parallel evolution of gene expression commonly underlies convergent niche specialization, but parallel changes in expression could also underlie divergent specialization. We investigated divergence in gene expression and whole-genome genetic variation across three sympatric Cyprinodon pupfishes endemic to San Salvador Island, Bahamas. This recent radiation consists of a generalist and two derived specialists adapted to novel niches - a scale-eater and a snail-eater. We sampled total mRNA from all three species at two early developmental stages and compared gene expression with whole-genome genetic differentiation among all three species in 42 resequenced genomes. 80% of genes that were differentially expressed between snail-eaters and generalists were up or downregulated in the same direction between scale-eaters and generalists; however, there were no fixed variants shared between species underlying these parallel changes in expression. Genes showing parallel evolution of expression were enriched for effects on metabolic processes, whereas genes showing divergent expression were enriched for effects on cranial skeleton development and pigment biosynthesis, reflecting the most divergent phenotypes observed between specialist species. Our findings reveal that even divergent niche specialists may exhibit convergent adaptation to higher trophic levels through shared genetic pathways. This counterintuitive result suggests that parallel evolution in gene expression can accompany divergent ecological speciation during adaptive radiation.\n\nImpact SummaryAdaptations that result in unique forms of ecological specialization are central to research in evolutionary biology, yet little is known about their molecular foundations. We combined transcriptome sequencing with whole-genome divergence scans to study the molecular evolution of two specialist Cyprinodon pupfish species - a scale-eater and a snail-eater - that rapidly diverged from a sympatric generalist ancestor within the last 10,000 years. While parallel evolution of gene expression driving convergent niche specialization seems common, we present, to our knowledge, the first example of significant parallel changes in expression coinciding with divergent niche specialization. 80% of genes that were differentially expressed between snail-eaters and generalists showed the same direction of expression in scale-eaters relative to generalists. Furthermore, parallel evolution in expression seem to be controlled by unique genetic variants in each specialist species. Genes showing parallel changes in expression were enriched for metabolic processes that may facilitate adaptation to a higher trophic level, while genes showing divergent expression likely shape the striking morphological differences between specialists. These findings contribute to a more nuanced understanding of convergent adaptations that arise during speciation, and highlight how species can evolve similar expression profiles adapted to divergent niches.

evolutionary biology↗

bioRxiv2017

Adaptive introgression from distant Caribbean islands contributed to the diversification of a microendemic radiation of trophic specialist pupfishes

Rapid diversification often involves complex histories of gene flow that leave variable and conflicting signatures of evolutionary relatedness across the genome. Identifying the extent and source of variation in these evolutionary relationships can provide insight into the evolutionary mechanisms involved in rapid radiations. Here we compare the discordant evolutionary relationships associated with species phenotypes across 42 whole genomes from a sympatric adaptive radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas and several outgroup pupfish species in order to understand the rarity of these trophic specialists within the larger radiation of Cyprinodon. 82% of the genome depicts close evolutionary relationships among the San Salvador Island species reflecting their geographic proximity, but the vast majority of the fixed variants between the specialist species lie in regions with discordant topologies. These regions include signatures of selective sweeps and adaptive introgression from neighboring islands into each of the specialist species. Hard selective sweeps of genetic variation on San Salvador contributed 10-fold more to divergence between specialist species within the radiation than adaptive introgression of Caribbean genetic variation; however, some of these introgressed regions from distant islands were associated with the primary axis of oral jaw divergence within the radiation. For example, standing variation in a proto-oncogene (ski) known to have effects on jaw size introgressed into one San Salvador specialist from an island 300 km away. The complex emerging picture of the origins of adaptive radiation on San Salvador indicates that multiple sources of genetic variation contributed to the adaptive phenotypes of novel trophic specialists on the island. Our findings suggest that a suite of factors, including rare adaptive introgression, may also be required to trigger adaptive radiation in the presence of ecological opportunity.\n\nAuthor summaryGroups of closely related species can rapidly evolve to occupy diverse ecological roles, but the ecological and genetic conditions that trigger this diversification are still highly debated. We examine patterns of molecular evolution across the genomes of a rapid radiation of pupfishes that includes two trophic specialists. Despite apparently widespread ecological opportunities and gene flow across the Caribbean, this radiation is endemic to a single Bahamian Island. Using the whole genomes of 42 pupfish we find evidence of extensive and previously unexpected variation in evolutionary relatedness among Caribbean pupfish. Two sources of genetic variation have contributed to the adaptive diversification of complex phenotypes in this system: selective sweeps of genetic variation from across the Caribbean that was brought into San Salvador through hybridization and genetic variation found on San Salvador. While genetic variation from San Salvador appears to be relatively more common in the divergence observed among specialists, hybridization probably played an important role in the evolution of the complex phenotypes as well. Our findings that multiple sources of genetic variation contribute to the San Salvador radiation suggest that a complex suite of factors, including hybridization with other species, may be required to trigger adaptive radiation in the presence of ecological opportunity.

evolutionary biology↗