Ancient climate changes and relaxed selection shape cave colonization in North American cavefishes

Area of Science:

• Evolutionary biology
• Genomics
• Paleoclimatology

Background:

• Extreme environments like caves offer insights into evolutionary processes.
• Cave colonization by organisms is a repeated phenomenon, but its timing and genetic basis are unclear.
• North American Amblyopsidae fishes provide a model system with surface, facultative, and obligate cave-dwelling species.

Purpose of the Study:

• To elucidate the evolutionary history and adaptive processes of cave colonization in Amblyopsidae fishes.
• To determine the timing and mode of independent cave colonizations.
• To investigate the genetic underpinnings of adaptation to cave environments.

Main Methods:

• Phylogenomic analysis using 1105 exon markers.
• Total-evidence dating incorporating fossil data.
• Palaeoclimatic modeling.
• Comparative genomic analysis of 487 candidate genes.

Main Results:

• A robust phylogeny confirmed the nested position of facultative cave-dwellers within blind cavefishes.
• Three independent cave colonizations were dated to the Early Miocene (18.5 Ma), Late Miocene (10.0 Ma), and Pliocene (3.0 Ma).
• Comparative genomics revealed both relaxed and intensified selection on genes related to troglomorphy, with a prevalence of relaxed selection supporting neutral mutation's role.

Conclusions:

• Cave colonization in Amblyopsidae is likely driven by climate change, supporting the climate-relict hypothesis.
• Neutral mutation plays a significant role in the evolution of cave-obligate species.
• The study offers insights into the complex selective pressures shaping life in extreme environments.