Abstract
Vertebrates acquired dim-light vision when an ancestral cone evolved into the rod photoreceptor at an unknown stage preceding the last common ancestor of extant jawed vertebrates (~420 million years ago Ma). The jawless lampreys provide a unique opportunity to constrain the timing of this advance, as their line diverged ~505 Ma and later displayed high-morphological stability. We recorded with patch electrodes the inner segment photovoltages and with suction electrodes the outer segment photocurrents of Lampetra fluviatilis retinal photoreceptors. Several key functional features of jawed vertebrate rods are present in their phylogenetically homologous photoreceptors in lamprey: crucially, the efficient amplification of the effect of single photons, measured by multiple parameters, and the flow of rod signals into cones. These results make convergent evolution in the jawless and jawed vertebrate lines unlikely and indicate an early origin of rods, implying strong selective pressure toward dim-light vision in Cambrian ecosystems.
Highlights
The fossil record shows that by the middle Cambrian, camera-type eyes were already present in stem vertebrates (Morris and Caron, 2014), supporting the emerging concept that spatially resolved vision provided a major competitive advantage in those biota (Paterson et al, 2011)
We made perforated patch-clamp recordings from photoreceptor inner segments and found that the dark membrane potential was of −43.2 ± 0.7 mV for short photoreceptors (SPs) (n = 30) and −45.9 ± 1.1 mV for long photoreceptors (LPs) (n = 10) (Table 1); these values are in line with those of jawed vertebrate rods and cones (Cangiano et al, 2012)
We examined lamprey SPs and LPs and found that their general properties closely match those of jawed vertebrate rods and cones: dark membrane potentials of around −45 mV, hyperpolarizing responses of up to 30 mV upon illumination, and the expression of a prominent hyperpolarization-activated Ih current are all typical traits of jawed vertebrate photoreceptors and must have been in place already by the middle Cambrian
Summary
The fossil record shows that by the middle Cambrian, camera-type eyes were already present in stem vertebrates (Morris and Caron, 2014), supporting the emerging concept that spatially resolved vision provided a major competitive advantage in those biota (Paterson et al, 2011). Current molecular genetic evidence indicates that modern rods evolved from an ancestral cone (Okano et al, 1992; Yokoyama, 2000; Lamb et al, 2007; Kawamura and Tachibanaki, 2008; Shichida and Matsuyama, 2009), implying that vision in near darkness is a relatively recent acquisition (Lamb, 2013) and causing the point of contention to become that of the timing of rod evolutionary emergence This advance must have occurred (i) after the appearance of the precursor of rhodopsin and of other rod-specific phototransduction proteins isoforms and (ii) before the initial diversification of extant jawed vertebrates (∼420 Ma; Erwin et al, 2011) endowed with modern rods.
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