Daphnia

Bellati, Adriana, Tiberti, Rocco, Cocca, Walter, Galimberti, Andrea, Casiraghi, Maurizio, Bogliani, Giuseppe & Galeotti, Paolo, 2014, A dark shell hiding great variability: a molecular insight into the evolution and conservation of melanic Daphnia populations in the Alps, Zoological Journal of the Linnean Society 171 (4), pp. 697-715 : 707-708

PIGMENTED DAPHNIA

Before the present study, melanic populations inhabiting alpine lakes were traditionally ascribed to D. middendorffiana , an arctic endemic that shares a dark cuticular pigmentation and obligate parthenogenesis with some rare high mountain populations ( Margaritora, 1985; Tiberti, 2011). Nevertheless, the unreliability of melanism for taxonomic assignment has been widely recognized by specialists (e.g. Glagolev, 1995; Kotov et al., 2010) and nowadays several case studies clearly point out the plastic nature of this feature (e.g. Daphnia longispina, Taylor, Hebert & Colbourne, 1996 ; Australian Daphnia spp. , Colbourne, Wilson & Hebert, 2006; North American Daphnia spp. , Colbourne et al., 1997; Arctic Daphnia spp. , Hessen et al., 1999; Daphnia obtusa Kurz, 1874 , Kotov & Taylor, 2010; Daphnia melanica Hebert, 1995 , Scoville & Pfrender, 2010). According to the literature, our molecular data show that melanic specimens found in the four alpine lakes overall differed by just 1% COI sequence variation from lowland transparent EuPC haplotypes. Moreover, in the light of phylogenetic evidences we can further confirm that dark phenotypes occur as a result of phenotypic plasticity in our alpine populations, indicating the need for morphological revision based on reliable diagnostic characters in future. Rather than high altitudes, strong UV exposure (coupled with the absence of visual predators, such as fish) was probably the primary determinant for the evolution of carapace pigmentation. Indeed, melanin is a photoprotective pigment ( Rhode, Pawlowski & Tollrian, 2001), which confers a substantial survival advantage to the individual not only at high altitudes or latitudes, but wherever concentrations of light-adsorbing matter in the water is extremely low (e.g. retrodunal sand ponds in temperate regions at low latitude, Miner et al., 2013). Our findings are also particularly useful from a genome- wise perspective because they add information on the selective forces and the parallel evolution of this adaptive trait within Daphnia and in very diversified evolutionary lineages of EuPC (both ‘Boreal’ and ‘Alpine’ clades). Similarly, the occurrence of an orange (carotenoid-pigmented) morphotype in the High Tatra (Lityn´ ski, 1917), and a black (melanin-pigmented) morphotype in glacial lakes in the Pyrenees ( Ventura & Catalan, 2005), both allied to the North American D. pulicaria (NAPC, Marková et al., 2007) , should be considered as a result of ecological convergence amongst deeply diversified clades (EuPC and NAPC) living in extreme glacial environments and arctic taxa (such as D. middendorffiana ).

Besides carapace melanization, we might further speculate that high-mountain populations may show other ecological peculiarities similar to arctic species and different from their conspecific transparent morphotype. Arctic populations are often obligately parthenogenetic, an extreme condition in which embryos develop directly by apomixes, with females producing viable diapause eggs (named ephippia) without males ( Hebert, 1981). To our knowledge, males were absent in our study lakes ( Tiberti, 2011) as well as in the other alpine population morphologically described as D. middendorffiana (Lake di Campo IV, 2293 m a.s.l. in the Bognanco Valley, Central Alps, Zaffagnini & Sabelli, 1972). Again, the extreme reproductive pattern observed may represent another convergent ecological trait between high mountain and arctic populations that should be regarded as ‘geographical parthenogenesis’ induced by very brief ice-free seasons, requiring fast production of diapause eggs ( Vandel, 1928). Concerning the present study, the discovery of monoclonal alpine populations in which a single haplotype was shared by all the individuals of the same lake further supports this conclusion. Noteworthily, obligate parthenogenesis within the D. pulex group may also be triggered by hybridization ( Innes & Hebert, 1988; Hebert & Finston, 2001), and actually High Tatra EuPC populations (the HTM haplogroup) display this particular reproduction mode as a result of past hybridization amongst deeply diversified glacial lineages ( Dufresne et al., 2011). As we looked only at mitochondrial variation here, we cannot rule out the possibility that a complex history of genetic introgression and reticulate evolution amongst divergent lineages inhabiting remote glacial areas also generated parthenogenesis in some alpine lakes. For instance, a similar scenario has been proposed to explain the evolution of obligate asexuality in eastern populations inhabiting the High Tatra Mountains ( Dufresne et al., 2011). Nevertheless, because distinct haplotypes have been found in a few alpine populations (i.e. population 9, see Fig. 3 ), we cannot rule out that cyclic parthenogenesis may also persist locally as a result of an ancient colonization event. Further studies involving nuclear markers (i.e. microsatellites) are currently ongoing and will allow the clarification of this issue from a population genetics perspective.

Figures

Figure 3. Map of the Alps showing European Daphnia pulicaria populations (1–12) and haplotypes (A1–A10) considered in this study. Different colours and patterns identify haplotypes found in more than one population or together with other haplotypes. See Table 1 for details of populations.