Wild fish thrive despite ‘hopeless monster’ mutations, Stanford-led study finds | Information Center

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“Lab-reared four-winged fruit flies are a famous example of how relatively simple genetic alterations in the regulatory regions of HOX genes can dramatically alter an animal’s body shape,” Kingsley said. “But because these flies cannot survive in the wild, anti-evolution proponents have seized on them – not as good examples of how genes drive evolution, but as proof that genetic changes can only make animals less functional.”

The two to four inch long sticklebacks, which sport a varying number of sharp spines along their backs, are excellent subjects for research because they evolve rapidly and dramatically in response to changing environmental conditions. A lake filled with piscivorous insects often harbors sticklebacks with fewer and shorter spines to grasp. But a pond with larger fish or birds that swallow their fish sticks whole is likely to boast a population of sticklebacks with longer, more throat-scratching spines. Aquatic weed forests are ideal for flexible, slippery fish that can hide in vegetation, while in the open sea, armored plates and fearsome spines are the way to go.

Kingsley’s lab began the study with aqueous matchmaking. Previous graduate students crossed a female twospine stickleback from a freshwater lake in British Columbia with a male threespine stickleback from the salt waters of Bodega Bay, California. They then crossed the offspring of this match to each other and analyzed the number and shape of their spines. Most of the 590 greatfish had three spines, but six had two spines and 21 had four spines – more than any of their ancestors. Extensive genetic studies in variable-spined fish have shown differences in the region around a gene called HOXDB, which is part of the HOX gene family.

A link between genes and anatomy

Wucherpfennig continued to collect and traverse sticklebacks from a myriad of North American lakes and streams, study their genetic makeup, and use CRISPR methods to confirm the effects of the HOXDB gene on spines. She found a panel of changes in regions near the HOXDB gene and showed that they were associated with major anatomical changes that evolve in the defensive armor of wild fish.

“In Nova Scotia, some of the stickleback populations have evolved to have five or even six spines,” Kingsley said. “Nature left the coding region of this gene intact, but changed the way and timing of its expression during normal development to add structures rather than remove them. And fish with these new structures thrive in an environment completely wild subject to a whole range of environmental pressures.

Wucherpfennig and her colleagues showed that repeated changes in regulatory regions of the HOXDB gene are responsible for the recent evolution of new spine patterns in two different stickleback species she studied across North America. They now want to know if similar changes are responsible for differences in fish that are even further apart.

“Are there predictable rules that govern evolutionary change?” said Kingsley. “Do natural species use the same trick over and over again or do they have to invent a new trick each time? Until now, it was the same gene, even in these highly divergent sticklebacks from different environments. Here we show that nature regularly adds major structures to generate animals that are more adapted to the environment, and that it does so repeatedly using the same master regulatory gene. This is a compelling argument for progressive evolution, debated in academic and non-academic circles for decades.

Researchers from Duke University School of Medicine, University of Victoria, UC Berkeley and Saint Mary’s University in Nova Scotia contributed to the study.

The research was supported by the National Institutes of Health (grants 2T32GM007790 and R01GM124330), the National Science Foundation, a Stanford Graduate Fellowship, a Helen Hay Whitney Postdoctoral Fellowship, the Natural Sciences and Engineering Research Council of Canada and the Howard Hughes Medical Institute.

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