Abstract
Phenotypic plasticity buffers organisms from environmental change and is hypothesized to aid the initial establishment of nonindigenous species in novel environments and postestablishment range expansion. The genetic mechanisms that underpin phenotypically plastic traits are generally poorly characterized; however, there is strong evidence that modulation of gene transcription is an important component of these responses. Here, we use RNA sequencing to examine the transcriptional basis of temperature tolerance for round and tubenose goby, two nonindigenous fish species that differ dramatically in the extent of their Great Lakes invasions despite similar invasion dates. We used generalized linear models of read count data to compare gene transcription responses of organisms exposed to increased and decreased water temperature from those at ambient conditions. We identify greater response in the magnitude of transcriptional changes for the more successful round goby compared with the less successful tubenose goby. Round goby transcriptional responses reflect alteration of biological function consistent with adaptive responses to maintain or regain homeostatic function in other species. In contrast, tubenose goby transcription patterns indicate a response to stressful conditions, but the pattern of change in biological functions does not match those expected for a return to homeostatic status. Transcriptional plasticity plays an important role in the acute thermal tolerance for these species; however, the impaired response to stress we demonstrate in the tubenose goby may contribute to their limited invasion success relative to the round goby. Transcriptional profiling allows the simultaneous assessment of the magnitude of transcriptional response as well as the biological functions involved in the response to environmental stress and is thus a valuable approach for evaluating invasion potential.
Highlights
| METHODSRound and tubenose gobies were collected in the first week of October 2014 from the Detroit River using a 10-m beach seine net
In recent decades, there has been renewed interest in phenotypic plasticity as a mechanism that facilitates species persistence in novel and changing environments (Ghalambor, McKay, Carroll, & Reznick, 2007)
To further facilitate comparison of gene transcription variation between species and allow combining the species-specific datasets, we identified putative orthologous genes using reciprocal best blast hits for round goby and tubenose goby transcripts using the blastn algorithm from BLAST+ v2.19 (Camacho et al, 2009)
Summary
Round and tubenose gobies were collected in the first week of October 2014 from the Detroit River using a 10-m beach seine net. We included only orthologous genes identified as statistically significantly responding to temperature challenge based on the two-factor GLMs. Here, we analyzed the paired comparison of Log fold changes between the two species of goby for upregulated and downregulated genes separately in each treatment with Wilcoxon signed-rank tests, a nonparametric analog of a paired t-test. Log fold changes were on average greater in magnitude for round goby in all comparisons except for genes upregulated in response to cold, where there was no significant difference (Table 1; Figure 3) This indicates that round goby have an increased scope for transcriptional plasticity compared with tubenose goby. Pattern of higher average transcription in tubenose goby is largely driven by differences in constitutive expression of genes not responding plastically to temperature challenge (Table 2), there is a significant difference in the magnitude of transcription between species for genes upregulated in response to decreased temperature. Round goby exhibited extreme plasticity for additional processes related to oxygen binding and carbohydrate metabolism, while tubenose goby exhibited plasticity for ceramide metabolic process potentially related to signaling cellular stress
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