An indigenous religious ritual selects for resistance to a toxicant in a livebearing fish

Abstract

Human-induced environmental change can affect the evolutionary trajectory of populations. In Mexico, indigenous Zoque people annually introduce barbasco, a fish toxicant, into the Cueva del Azufre to harvest fish during a religious ceremony. Here, we investigated tolerance to barbasco in fish from sites exposed and unexposed to the ritual. We found that barbasco tolerance increases with body size and differs between the sexes. Furthermore, fish from sites exposed to the ceremony had a significantly higher tolerance. Consequently, the annual ceremony may not only affect population structure and gene flow among habitat types, but the increased tolerance in exposed fish may indicate adaptation to human cultural practices in a natural population on a very small spatial scale.

Translocation of cave fish (Poecilia mexicana) within and between natural habitats along a toxicity gradient

“…In summary, our experiments indicate that under certain conditions (i.e., gradual transfer along the gradient from toxic to nontoxic), factors other than toxicity must also play an important role in maintaining reproductive isolation reported on by previous studies (Plath et al 2007aTobler et al 2008a). Clearly, sudden translocation as it is possible during extreme flooding events or human-induced translocation during a religious ceremony, in which cave fishes are poisoned and immobilized resulting in passive downstream drifting (Tobler et al 2011a), is not likely to lead to successful gene flow due to the high mortality induced by rapid translocation between extreme and benign environments ). Under the scenario that we investigated here that envisions gradual movement along a gradient allowing for potential acclimatisation, previously described additional selective forces acting against migrants (e.g., predation: Tobler 2009;Riesch et al 2010a; sexual selection: Tobler et al 2008b) are likely to contribute more to reproductive isolation than previously assumed (Tobler 2009).…”

“…) or human‐induced translocation during a religious ceremony, in which cave fishes are poisoned and immobilized resulting in passive downstream drifting (Tobler et al. ), is not likely to lead to successful gene flow due to the high mortality induced by rapid translocation between extreme and benign environments (Tobler et al. ).…”

Gradient Evolution of Body Colouration in Surface- and Cave-DwellingPoecilia mexicanaand the Role of Phenotype-Assortative Female Mate Choice

“…Here, populations of the live-bearing fish Poecilia mexicana inhabit environments characterized by all possible combinations of two extreme environmental factors: a sulphidic cave (Cueva del Azufre), a nonsulphidic cave (Cueva Luna Azufre), a sulphidic surface river (El Azufre), and several nonsulphidic, normoxic rivers and creeks [17]. This has led to pronounced phenotypic divergence in several behavioural (e.g., [13, 33–37]), dietary [38, 39], female and male life-history [40–42], morphological [2, 43], and physiological traits [44, 45]. Nevertheless, photoreceptors in cave and surface-dwelling fish appear to be functionally unchanged because spectral sensitivities are virtually identical [46].…”

“…For centuries the Zoque indigenous people have conducted a fertility ceremony (“La Pesca”) during the holy week before Easter, in which they use barbasco plant roots ( Lonchocarpus sp., Fabaceae) that contain the fish-toxin rotenone to poison cave fish. The anaesthetized fish are drifted outside the cave where they are then collected and eaten [44]; not all sedated fish are captured though, and some recovering individuals might still be able to reproduce. However, this raises the question of why gene flow is surprisingly low despite this massive perturbation every year through the flush of fish out of the cave?…”

Peer Review #2 of "Microhabitat use, population densities, and size distributions of sulfur cave-dwelling Poecilia mexicana (v0.1)"

“…One factor that most likely influences population dynamics is the annual 'La Pesca' ceremony. The ceremony leads to a strong temporary reduction of local fish densities in those cave chambers that are situated downstream of the barbasco release site (Tobler et al 2011a). Our study was conducted approximately nine months after the last ceremony, but given rather long generation times in P. mexicana (roughly 3-6 months for males and 7-10 months for females from birth until reaching maturation under common-garden rearing conditions; Riesch, Reznick, Plath & Schlupp, submitted), we predicted to find lower (sub-)population densities and especially fewer large-bodied individuals downstream of the site in the Cueva del Azufre where barbasco is annually released.…”