Photoperiodic response of sexual reproduction in the Daphnia pulex group is reversed in two distinct habitats

Two traditional species in the Daphnia pulex group (0. pulex and D. pulicmiu) are not completely reproductively isolated. The microhabitats they dominate are distinct but overlap geographically, and migration between the microhabitats is not uncommon. Their species identity is not fully supported by a recent molecular study. A laboratory experiment shows that Daphnia clones isolated from two populations of each species switch to sexual reproduction in response to totally different photoperiodic cues, so that their mating seasons are expected to differ. This phenomenon is most likely due to local adaptation of the two species to their respective distinct microhabitats. The phenomenon, together with the peculiarity of the study system, is interpreted as an ongoing allochronic speciation process in aquatic systems. Much has been debated about the origin of species, and the mode of sympatric speciation is particularly contentious (White 1978; Bush 1994). Allochronic speciation is a special form of sympatric speciation, in which differences in mating season contribute to the divergence of two taxa that may interbreed otherwise (White 1978). In animals, there are a few cases in which allochronic speciation is thought to occur, all of which are from terrestrial systems (White 1978). Here I report the results from an experiment with the freshwater microcrustacean Daphnia and interpret the results in light of the possibility of allochronic speciation in this aquatic system. The Daphnia p&x group consists of obligately asexual and cyclically parthenogenetic populations. Cyclically parthenogenetic populations normally reproduce asexually during the growing season in benign environments and produce diapausing eggs (ephippia) sexually prior to the arrival of seasonally harsh periods (e.g. drought in summer in temporary ponds and adverse winters in permanent lakes). Seasonal timing of sexual reproduction is important in determining an individual’s fitness (Carvalho and Hughes 1983; Hobaek and Larsson 1990), which is more or less synchronized in a particular season within populations (Stross 1987; Threlkeld 1987) and has a genetic basis (Carvalho and Hughes 1983; Yampolsky 1992; Deng 1996). Two traditional species within the D. p&x group (0. p&x and D. pulicaria) normally live in distinct but geographically overlapping habitats. D. pulex occupies temporary ponds and D. pulicaria inhabits permanent lakes. The two species are morphologically similar (Brandlova et al. 1972) but are fixed for alternative alleles at the diagnostic lactate dehydrogenase (LDH) locus (Hebert et al. 1988, 1989; Lynch et al. 1989). Mating is normally random within cyclically parthenogenetic populations of the two species (Lynch and Spitze 1994; Lynch and Deng 1994; Deng and Lynch 1996). Interbreeding between the two species is not uncommon in nature; hybrids are viable and fertile (Hebert 1987; Hebert and Crease 1980, 1983) but normally reproduce purely asexually (Crease et al. 1990). Genetic inh-ogression between the two species is rare (Cemy and Hebett 1993). A recent molecular phylogenetic study does not support the conclusion that these two traditional taxa are distinct species (Lehman et al. 1995). Populations of traditional D. pulex and D. pulicaria are widely distributed in midwest Oregon. Their habitats overlap geographically and have distinct phenologies. The temporary ponds inhabited by D. pulex usually begin to fill with water by spring and dry up in summer, whereas the populations of D. pulicaria in permanent habitats (lakes and reservoirs) usually decline in autumn. Co-occurrence of the two species in a single pond or lake has not yet been found in midwest Oregon, although it has been reported elsewhere (Cemy and Hebert 1993). To investigate the patterns of sexual reproduction in different seasons, I examined four populations in midwest Oregon under different photoperiods. I found that sexual reproduction was induced in D. pulicaria from permanent habitats by short-day photoperiods and in D. pulex from temporary ponds by long-day photoperiods. The opposite photoperiodic responses are adaptive with regard to the respective dominant habitats of the two species. The phenomenon should promote sexual reproduction in different seasons and serve as a premating isolating mechanism, thus reducing gene flow between the two species. All four experimental populations are within -250 km of each other. Two populations of D. pulicaria were collected from permanent habitats (Little Cultus Lake in the Oregon Cascades and Dorena Reservoir in the Willamete Valley). Two D. pulex populations were collected from temporary ponds on the Oregon Coast (Haceta Pond and Florence Dune Pond). According to the traditional criteria (Brooks 1957; Hebert et al. 1988, 1989; Lynch et al. 1989), the two permanent populations were classified as D. pulicuria and the two temporary pond populations as D. pulex. Consistency with Hardy-Weinberg proportions at the polymorphic loci phosphoglucomutase (PGM) and phosphoglucoisomerase (PGI) revealed that these four populations are cyclically parthenogenetic and mating is effectively random within each population (Deng unpubl.). Dozens of random individuals from each population were isolated into small individual beakers containing about 200 ml of water from Dorena Reservoir The isolated individuals were fed with the green alga Scenedesmus and kept at 15°C and 12: 12 L/D photoperiod. All isolates reproduced asexually in the laboratory and formed clonal cultures. Twenty clones from each of the four populations were used in the following experiment. I assumed that a day consisted of the hours between sunrise and sunset and chose four photoperiods (10, 13.5, 15.5, 17 h of light d-l) to cover all seasons experienced in nature at 42-46”N. Within each photoperiod, each clone of each population was represented by two replicates. Each replicate was initiated by one immature individual from its clonal culture as the first generation; two newborns from the first clutch of the first generation were used to start