Maya S. Enriquez’s research while affiliated with University of Minnesota and other places

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Publications (4)


Mutations in the albinism gene oca2 alter vision-dependent prey capture behavior in the Mexican tetra
  • Article

March 2025

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31 Reads

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1 Citation

Journal of Experimental Biology

Stefan Choy

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Sunishka Thakur

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Ellen Polyakov

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[...]

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Johanna E Kowalko

Understanding the phenotypic consequences of naturally occurring genetic changes, as well as their impact on fitness, is fundamental to understanding how organisms adapt to an environment. This is critical when genetic variants have pleiotropic effects, as determining how each phenotype impacted by a gene contributes to fitness is essential to understand how and why traits have evolved. Here, we characterize the effects of mutations in the oca2 gene, coding mutations in which underlie albinism and reductions of sleep in the blind Mexican cavefish Astyanax mexicanus, on larval prey capture. We find that when surface A. mexicanus with engineered mutations in oca2 are hunting, they use cave-like, wide angle strikes to capture prey. However, unlike cavefish or surface fish in the dark, which utilize the lateral line when hunting, oca2 mutant (oca2Δ2bp/Δ2bp) surface fish can use vision when striking at prey from wide angles. We find that when raised under lighted conditions, pigmented surface fish outcompete albino oca2Δ2bp/Δ2bp surface fish when hunting in lighted conditions. In contrast, when surface fish are reared in darkness, oca2Δ2bp/Δ2bp surface fish outcompete their wild type siblings in the dark. This raises the possibility that albinism is detrimental to larval feeding in a surface-like lighted environment, but may confer an advantage to fish in cave-like, dark environments. Together, these results demonstrate that oca2 plays a role in larval feeding behavior in A. mexicanus, and expand our understanding of the pleiotropic phenotypic consequences of oca2 in cavefish evolution.


Figure 2 -oca2 mutant surface fish do not alter their strike dynamics in the dark. (A) Average 431 strike angles of wild-type (oca2 +/+ ) oca2 Δ2bp/Δ2bp surface fish in light and dark conditions. Welch's 432 t test: oca2 +/+ , light, (n = 15) and dark (n = 13), p<0.0001. t test: oca2 Δ2bp/Δ2bp , light (n = 19) and 433 dark (n = 14), p = 0.7862. (B) Average strike distances of wild-type and oca2 Δ2bp/Δ2bp surface fish 434 in light and dark conditions. Welch's t test: oca2 +/+ , light, (n = 15) and dark (n = 13), p = 0.5856. t 435 test: oca2 Δ2bp/Δ2bp , light (n = 19) and dark (n = 14), p = 0.3007. (C) Total number of strikes in 436 wild-type and oca2 Δ2bp/Δ2bp surface fish in light and dark conditions. Mann-Whitney U test: 437 oca2 +/+ , light, (n = 15) and dark (n = 13), p = 0.0001. Welch's t test: oca2 Δ2bp/Δ2bp , light (n = 19) 438 and dark (n = 14), p = 0.6401. (D) Success rates of wild-type and oca2 Δ2bp/Δ2bp surface fish in 439 light and dark conditions. Welch's t test: oca2 +/+ , light, (n = 15) and dark (n = 13), p = 0.0208. t 440 test: oca2 Δ2bp/Δ2bp , light (n = 19) and dark (n = 14), p = 0.1804. All error bars are standard error of 441 the mean. *p<0.05, **p<0.01, ***p<0.001, ****p<0.0001 442
Figure 4 -Competition assays reveal differences in hunting success between populations. (A) 490 Representative image of competition assay with a surface fish and Pachón cavefish. (B) 491 Proportion of total prey captured by surface fish competitors in a competition assay between a 492 surface fish and Pachón cavefish in light and dark conditions. One-Sampled T test, n = 20 trials 493 (light), 22 (dark), theoretical mean = 0.5, actual means = 0.7492 (light), 0.3841 (dark), t = 5.405 494 (light), 2.728 (dark), df = 19 (light), 21 (dark), p <0.0001 (light), 0.0126 (dark). (C) Proportion of 495 totally prey captured by pigmented surface fish sibling competitors (oca2 Δ2bp/+ or oca +/+ ) in a 496 competition assay between a pigmented surface fish and an oca2-mutant albino surface fish in 497 light and dark conditions. One-Sampled T test, n = 13 trials (light), 15 (dark), theoretical mean = 498 0.5, actual means = 0.7929 (light), 0.5934 (dark), t = 7.053 (light), 1.723 (dark), df = 12 (light), 499 14 (dark), p = <0.0001 (light), 0.1069 (dark). All error bars are standard error of the mean. 500 *p<0.05, **p<0.01, ***p<0.001, ****p<0.0001 501
Figures and Legends 411
Mutations in the albinism gene oca2 alter vision-dependent prey capture behavior in the Mexican tetra
  • Preprint
  • File available

June 2024

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30 Reads

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2 Citations

Understanding the phenotypic consequences of naturally occurring genetic changes, as well as their impact on fitness, is fundamental to understanding how organisms adapt to an environment. This is critical when genetic variants have pleiotropic effects, as determining how each phenotype impacted by a gene contributes to fitness is essential to understand how and why traits have evolved. A striking example of a pleiotropic gene contributing to trait evolution is the oca2 gene, coding mutations in which underlie albinism and reductions of sleep in the blind Mexican cavefish, Astyanax mexicanus. Here, we characterize the effects of mutations in the oca2 gene on larval prey capture. We find that when conspecific surface fish with engineered mutations in the oca2 allele are hunting, they use cave-like, wide angle strikes to capture prey. However, unlike cavefish or surface fish in the dark, which rely on lateral line mediated hunting, oca2 mutant surface fish use vision when striking at prey from wide angles. Finally, we find that while oca2 mutant surface fish do not outcompete pigmented surface siblings in the dark, pigmented fish outcompete albino fish in the light. This raises the possibility that albinism is detrimental to larval feeding in a surface-like lighted environment, but does not have negative consequences for fish in cave-like, dark environments. Together, these results demonstrate that oca2 plays a role in larval feeding behavior in A. mexicanus. Further, they expand our understanding of the pleiotropic phenotypic consequences of oca2 in cavefish evolution.

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The effects of intensive trapping on invasive round goby densities

May 2024

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57 Reads

The round goby (Neogobius melanostomus) is an invasive benthic fish first introduced to the Laurentian Great Lakes in 1990 that has negatively impacted native fishes through increased competition for food and habitat, aggressive interactions, and egg predation. While complete eradication of the round goby is currently not possible, intensive trapping in designated areas during spawning seasons could potentially protect critical native fish spawning habitats. Baited minnow traps were spaced 10 meters apart in shallow water along a 100-meter stretch of shoreline within the Duluth-Superior Harbor during the round goby breeding period (June to October) with captured round gobies removed from interior traps (N = 10) every 48 hours. These traps were bracketed by two pairs of reference traps deployed weekly for 48 hours, from which round gobies were also tagged and released. The number of round gobies captured in the interior traps declined by 67% compared to reference traps over the course of the study, with extended periods of no captures. The tagged round gobies showed high site affinity, with 82.8% of tagged fish recaptured at the previous release site. The results indicate that even at open water sites, which allow natural migration of round gobies into the area, extensive trapping could reduce local population numbers.


Geographic locations of recently invaded population sampling. Five recently invaded populations of Astyanax mexicanus found in the Edwards-Trinity Aquifier system were sampled for this study, with collection points indicated on the map. The triangle shape indicates both a surface and cave environment. Circles indicate intermediate environments, while a square indicates a surface environment.
Auditory evoked potentials. (A) Schematic of auditory evoked potential (AEP) experimental setup. (B–D) Median auditory sound pressure level (±SE) sensitivity compared between populations. (B) Comparison between Honey Creek Cave (blue circle) and Honey Creek Surface (yellow square). Asterisks (*) indicate a significant difference (Mann-whitney U test, p < 0.05) between populations. (C) Comparison between San Antonio Zoo (grey circle), Blue Hole (cyan square) and San Pedro Springs (magnenta triangle). Asterisks (*) indicate a significant (Kruskal-Wallis with post-hoc pairwise Wilcox w/Holm correction, p < 0.05) difference between San Antonio Zoo and Blue Hole. A black circle (•) indicates a significant difference between San Antonio Zoo and San Pedro Springs. (D) Comparison between Mexican Surface (red circle), Molino Cave (black square) and Pachon Cave (blue traingle). A significant difference is defined as p < 0.05 using a Kruskal-Wallis test with post-hoc pairwise Wilcox w/ Holm adjustment. Asterisks (*) indicate a significant difference between Mexican surface and Pachon Cave. A black circle (•) indicates a significant difference between Mexican surface and Molino Cave. A diamond (◊) indicates significant differences between all pairwise population comparisons.
Wild caught and lab-raised AEP Thresholds. (A–C) Median auditory sound pressure level (±SE) sensitivity compared between populations. (A) Comparison between wild-caught (red circle) and lab-raised (brown square) Honey Creek Surface fish. Asterisks (*) indicates significant (Mann-whitney U test, p < 0.05) difference between populations. (B-C) All frequencies tested show significant differences (Welch’s T test, p < 0.05) between populations unless marked with “ns”, indicating no significant difference. (B) Comparison between wild-caught (light blue) and lab-raised (beige square) Honey Creek Cave fish. (C) Comparison between wild-caught (dark blue circle) and lab-raised (green square) Blue Hole fish.
Particle acceleration levels. (A) Schematic of particle acceleration level (PAL) experimental setup. (B–D) Median auditory particle acceleration level (±SE) sensitivity compared between populations. (B) Comparison between Honey Creek Cave (dark blue circle) and Honey Creek surface (yellow square); asterisks (*) indicates a significant difference (Mann-Whitney U Test, p < 0.05) between populations. (C) Comparison between San Antonio Zoo (grey circle), Blue Hole (cyan square) and San Pedro Springs (magnenta triangle); A significant difference is defined as p < 0.05 using a Kruskal-Wallis test with post-hoc pairwise Wilcox w/ Holm Adjustment. Asterisks (*) indicate a significant difference between San Antonio Zoo and Blue Hole. A black circle (•) indicates a significant difference between San Antonio Zoo and San Pedro Springs. (D) Comparison between Mexican Surface (red circle), Molino Cave (black square) and Pachon Cave (blue traingle). A significant difference is defined as p < 0.05 using a Kruskal-Wallis test with post-hoc pairwise Wilcox w/ Holm adjustment. Asterisks (*) indicate a significant difference between Mexican surface and Pachon Cave. A black circle (•) indicates a significant difference between Mexican surface and Molino Cave.
Wild-caught and lab-raised PAL thresholds. (A–C) Median auditory particle acceleration sensitivity (±SE) between wild-caught and lab-raised populations. Asterisks (*) indicate significant (Mann–Whitney U Test, p < 0.05) differences between populations. (A) Comparison between wild-caught (red circle) and lab-raised (brown square) Honey Creek Surface fish. (B) Comparison between wild-caught (light blue) and lab-raised (beige square) Honey Creek Cave fish. (C) Comparison between wild-caught (dark blue circle) and lab-raised (green square) Blue Hole Fish.
Evidence for rapid divergence of sensory systems between Texas populations of the Mexican tetra (Astyanax mexicanus)

February 2023

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73 Reads

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2 Citations

Population divergence is often quantified using phenotypic variation. However, because sensory abilities are more difficult to discern, we have little information on the plasticity and rate of sensory change between different environments. The Mexican tetra (Astyanax mexicanus) is a fish distributed throughout Southern Texas and Northern Mexico and has evolved troglomorphic phenotypes, such as vestigial eyes and reduced pigmentation, when surface ancestors invaded caves in the past several hundred thousand years. In the early 1900s, surface A. mexicanus were introduced to the karstic Edwards-Trinity Aquifer in Texas. Subsequent cave colonization of subterranean environments resulted in fish with phenotypic and behavioral divergence from their surface counterparts, allowing examination of how new environments lead to sensory changes. We hypothesized that recently introduced cave populations would be more sensitive to light and sound when compared to their surface counterparts. We quantified divergence using auditory evoked potentials (AEPs) and particle acceleration levels (PALs) to measure differences in sound sensitivity, and electroretinography (ERGs) to measure light sensitivity. We also compared these results to measurements taken from native populations and lab-born individuals of the introduced populations. Honey Creek Cave fish were significantly more sensitive than proximate Honey Creek surface fish to sound pressure levels between 0.6 and 0.8 kHz and particle acceleration levels between 0.4 and 0.8 kHz. Pairwise differences were found between San Antonio Zoo surface and the facultative subterranean San Pedro Springs and Blue Hole populations, which exhibited more sensitivity to particle acceleration levels between 0.5 and 0.7 kHz. Electroretinography results indicate no significant differences between populations, although Honey Creek Cave fish may be trending toward reduced visual sensitivity. Auditory thresholds between wild-caught and lab-raised populations of recently invaded fish show significant differences in sensitivity, suggesting that these traits are plastic. Collectively, while these results may point to the rapid divergence of A. mexicanus in cave habitats, it also highlights the responsive plasticity of A. mexicanus auditory system to disparate environments.

Citations (2)


... Additionally, we assessed optomotor response (OMR) in pde6c CRISPant fish and their wild-type siblings. OMR assays are used in zebrafish and Mexican tetra as visual defect detection assay (LeFauve et al. 2021;Choy et al. 2024). OMR is an innate, orienting behavior evoked by whole-field visual motion, in our case, contrasting black and white lines that move across a screen. ...

Reference:

Population Genomics of Premature Termination Codons in Cavefish With Substantial Trait Loss
Mutations in the albinism gene oca2 alter vision-dependent prey capture behavior in the Mexican tetra

... Surface-dwelling morphs ( Figure 1b) reside in lakes, rivers, and streams throughout northeastern Mexico and the southern United States (Enriquez et al., 2023). Cave-dwelling morphs (Figure 1b) are distributed among over 30 limestone karsts in cave complexes including those of the Sierra de El Abra in northeastern Mexico ( Figure 1a) (Miranda-Gamboa et al., 2023). ...

Evidence for rapid divergence of sensory systems between Texas populations of the Mexican tetra (Astyanax mexicanus)