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Field studies reveal strong postmating isolation between ecologically divergent butterfly populations.

ABSTRACT: Gene flow between populations that are adapting to distinct environments may be restricted if hybrids inherit maladaptive, intermediate phenotypes. This phenomenon, called extrinsic postzygotic isolation (EPI), is thought to play a critical role in the early stages of speciation. However, despite its intuitive appeal, we know surprisingly little about the strength and prevalence of EPI in nature, and even less about the specific phenotypes that tend to cause problems for hybrids. In this study, we searched for EPI among allopatric populations of the butterfly Euphydryas editha that have specialized on alternative host plants. These populations recall a situation thought typical of the very early stages of speciation. They lack consistent host-associated genetic differentiation at random nuclear loci and show no signs of reproductive incompatibility in the laboratory. However, they do differ consistently in diverse host-related traits. For each of these traits, we first asked whether hybrids between populations that use different hosts (different-host hybrids) were intermediate to parental populations and to hybrids between populations that use the same host (same-host hybrids). We then conducted field experiments to estimate the effects of intermediacy on fitness in nature. Our results revealed strong EPI under field conditions. Different-host hybrids exhibited an array of intermediate traits that were significantly maladaptive, including four behaviors. Intermediate foraging height slowed the growth of larvae, while intermediate oviposition preference, oviposition site height, and clutch size severely reduced the growth and survival of the offspring of adult females. We used our empirical data to construct a fitness surface on which different-host hybrids can be seen to fall in an adaptive valley between two peaks occupied by same-host hybrids. These findings demonstrate how ecological selection against hybrids can create a strong barrier to gene flow at the early stages of adaptive divergence.

SUBMITTER: McBride CS

PROVIDER: S-EPMC2964332 | biostudies-literature | 2010 Oct

REPOSITORIES: biostudies-literature

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Field studies reveal strong postmating isolation between ecologically divergent butterfly populations.

McBride Carolyn S CS Singer Michael C MC

PLoS biology 20101026 10

Gene flow between populations that are adapting to distinct environments may be restricted if hybrids inherit maladaptive, intermediate phenotypes. This phenomenon, called extrinsic postzygotic isolation (EPI), is thought to play a critical role in the early stages of speciation. However, despite its intuitive appeal, we know surprisingly little about the strength and prevalence of EPI in nature, and even less about the specific phenotypes that tend to cause problems for hybrids. In this study, ...[more]

PMID: 21048982

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Project description:BackgroundAs ectothermic organisms have evolved to differing aquatic climates, the molecular basis of thermal adaptation is a key area of research. In this study, we tested for differential transcriptional response of ecologically divergent populations of redband trout (Oncorhynchus mykiss gairdneri) that have evolved in desert and montane climates. Each pure strain and their F1 cross were reared in a common garden environment and exposed over four weeks to diel water temperatures that were similar to those experienced in desert climates within the species' range. Gill tissues were collected from the three strains of fish (desert, montane, F1 crosses) at the peak of heat stress and tested for mRNA expression differences across the transcriptome with RNA-seq.ResultsStrong differences in transcriptomic response to heat stress were observed across strains confirming that fish from desert environments have evolved diverse mechanisms to cope with stressful environments. As expected, a large number of total transcripts (12,814) were differentially expressed in the study (FDR ≤ 0.05) with 2310 transcripts in common for all three strains, but the desert strain had a larger number of unique differentially expressed transcripts (2875) than the montane (1982) or the F1 (2355) strain. Strongly differentiated genes (>4 fold change and FDR ≤ 0.05) were particularly abundant in the desert strain (824 unique contigs) relative to the other two strains (montane = 58; F1 = 192).ConclusionsThis study demonstrated patterns of acclimation (i.e., phenotypic plasticity) within strains and evolutionary adaptation among strains in numerous genes throughout the transcriptome. Key stress response genes such as molecular chaperones (i.e., heat shock proteins) had adaptive patterns of gene expression among strains, but also a much higher number of metabolic and cellular process genes were differentially expressed in the desert strain demonstrating these biological pathways are critical for thermal adaptation to warm aquatic climates. The results of this study further elucidate the molecular basis for thermal adaptation in aquatic ecosystems and extend the potential for identifying genes that may be critical for adaptation to changing climates.

Project description:Crustaceans are generally considered more sensitive to ocean warming due to their lack of certain efficient regulators. However, the alterations in the physiology and behavior of crustaceans in response to thermal stress differ vastly even among the infraspecific populations of heterogeneous landscapes. Consequently, understanding the impact of temperature fluctuation on crustacean infraspecific populations might be essential for maintaining a sustainable persistence of populations at existing locations. In the present study, we chose the Japanese mantis shrimp (Oratosquilla oratoria) as the representative crustacean population, and conducted transcriptome analyses in two divergent O. oratoria populations (the Zhoushan and Qingdao populations) under same thermal stress (20-28 °C) to identify the population-specific expression response to thermal stress. The results showed significant differences in gene expressions, GO terms and metabolic pathways between the two populations. We hypothesized that intraspecific mutations in the same or different genes might lead to thermal adaptive divergences. Temperature increases from 20-28 °C produced significant enrichment in GO terms and altered the metabolic pathways in the Zhoushan population despite the lack of differentially expressed unigenes. Therefore, several functional genes with large pleiotropic effects may underlie the response to thermal stress in the Zhoushan population. Furthermore, the most significantly enriched biological processes of the Qingdao population were associated with the state or activity of cells and its significant enriched pathways with genetic information processing as well as immune and environmental information processing. In contrast, the differentially regulated unigenes of the Zhoushan population were primarily involved in the regulatory cellular and transcription processes and the most significant pathways found were metabolic and digestive. Consequently, the regulatory mechanisms of the Zhoushan population are probably more efficient than those of the Qingdao population under the same thermal stress.

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Field studies reveal strong postmating isolation between ecologically divergent butterfly populations.

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Field studies reveal strong postmating isolation between ecologically divergent butterfly populations.

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