Biology subjects

McGirr, J. A.

Publications and source records attributed to McGirr, J. A..

4 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

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

The Rate Of Evolution Of Postmating-Prezygotic Reproductive Isolation In Drosophila

Reproductive isolation (RI) is an intrinsic aspect of species, as described in the Biological Species Concept. For that reason, the identification of the precise traits and mechanisms of RI, and the rates at which they evolve, is crucial to understanding how species originate and persist. Nonetheless, precise measurements of the magnitude of reproductive isolation are rare. Previous work has measured the rates of evolution of prezygotic and postzygotic barriers to gene flow, yet no systematic analysis has carried out the study of the rates of evolution of postmating-prezygotic (PMPZ) barriers. We systematically measured the magnitude of two barriers to gene flow that act after mating occurs but before zygotic fertilization and also measured a premating (female mating rate in nonchoice experiments) and two postzygotic barriers (hybrid inviability and hybrid sterility) for all pairwise crosses of species within the Drosophila melanogaster subgroup. Our results indicate that PMPZ isolation evolves faster than hybrid inviability but slower than premating isolation. We also describe seven new interspecific hybrids in the group. Our findings open up a large repertoire of tools that will enable researchers to manipulate hybrids and explore the genetic basis of interspecific differentiation, reproductive isolation, and speciation.

evolutionary biology↗