Incipient regressive evolution of the circadian rhythms of a cave amphipod

Abstract

The habitat of cave-adapted organisms is characterized by complete darkness and in some instances, an apparent lack of environmental distinction between day and night. It is unclear if cave-adapted organisms retain circadian rhythms that can be light-entrained. Stygobromus allegheniensis (Allegheny Cave Amphipod) is an eyeless troglobitic crustacean found in caves located in the Northeastern region of the United States. Two cave populations were examined for evidence of light-entrained circadian rhythms. The first population inhabits a small tectonic cave (Ice Caves, Sam's Point Preserve, NY) and the second (Clarksville Cave, Clarksville, NY) inhabits a long cave system in limestone rock. Experiments conducted in both the field and the laboratory suggest that the capacity to exhibit motor rhythms has been conserved in at least some individuals of both populations. Nonetheless, their motor activity rhythms have high variability of period length between individuals and do not appear to be light-entrainable. It is thus proposed that in this species, light-entrainable circadian rhythms controlling motor activity have undergone incipient regressive evolution.

Day–night and seasonal variations of a subterranean invertebrate community in the twilight zone

“…As a direct consequence of the lack of solar irradiation, primary phototrophic producers are absent in the deep parts of the caves, with the exception of plant roots growing from the soil into sub-superficial subterranean habitats (Gibert and Deharveng 2002). The permanent darkness below the ground also determines the absence of daily dark-light cycles and a reduced influence of the environmental cyclicity (Poulson and White 1969, Howarth 1980, 1983, two factors which seemingly triggered the reduction in the circadian components of activity of numerous cave-limited species over their evolutionary history (Trajano and Menna-Barreto 1995, Hervant et al 2000, Trajano et al 2005, Moran et al 2014, Espinasa et al 2016. As such, the subterranean domain is generally regarded as temporally stable.…”

Phylogenetically independent behavior mediating geographic distributions suggests habitat is a strong driver of phenotype in crangonyctid amphipods

“…Lower fitness of subterranean fauna in epigean habitats is likely due to a lack of sight, pigment, and camouflage, increasing vulnerability to predation (Tobler, 2009;Horstkotte et al, 2010;Klaus and Plath, 2011) and mutagenic radiation (Protas and Patel, 2008;Bilandzǐja et al, 2017). Likewise, epigean species are considered maladapted to subterranean environments due to the metabolic cost of maintaining eyes in the absence of light (Moran et al, 2015), higher metabolic rates and an inability to deal with prolonged periods of starvation due to scarcity of food in resource-limited subterranean environments (Aspiras et al, 2015;Nair et al, 2020), disruption of circadian rhythms (Espinasa et al, 2016), and difficulty finding mates (Riesch et al, 2011). Thus, fitness costs associated with surface-and subsurface-adapted taxa dispersing out of their respective habitats likely mediates contemporary biogeographic distributions to some extent.…”

“…This family of amphipods was selected because some species have eyes and live in epigean environments while others are eyeless, and the eyeless species occupy different microhabitats with differing light availability (Gibson et al, 2008). Also, eyeless stygobiontic amphipods in this family (i.e., Stygobromus allegheniensis) (Espinasa et al, 2016) and all the species in the stygobiontic genus Niphargus (Simcǐčand Brancelj, 2007;Borowsky, 2011;Fisěr et al, 2016) have the capacity to detect light despite vestigial or no eyes. To assess photophilia, photoneutrality, and photophobia, we performed experiments that quantified behavioral avoidance of direct light, and physiological stress response due to exposure to light.…”