Population genetic dynamics during colonisation and establishment of an obligate parthenogenetic Daphnia pulex population in a small lake of a continental archipelago

Abstract

Population genetic diversity and structure are known to influence successful colonisation and establishment of a population in a novel habitat. However, our understanding of actual population genetic changes in the early stage of colonisation and detailed time‐series of genetic changes during the establishment of a new population is still limited due to the difficulty of making long‐term direct observations of a colonising population. Using a paleolimnological approach, we revealed the long‐term genetic dynamics of an obligate parthenogenetic panarctic Daphnia pulex population during the early stage of colonisation and subsequent establishment in Lake Fukami‐ike of Nagano, Japan. We collected diapausing eggs in ephippia of D. pulex from layers of sediment core samples (c. 370 cm long; dated 1662–2017) and then the mitochondrial DNA was sequenced using the markers designed for the NADH dehydrogenase 5 (ND5) gene and the control region. Daphnia pulex colonised and established a population in the early 2000s. Population genetic analysis showed that one colonising haplotype predominated in the population throughout the study period. Genetic diversity was consistently limited and there was no recovery of genetic diversity after colonisation. Clearly limited genetic diversity did not hamper population growth, possibly because phenotypic plasticity was used to cope with changes in predation pressure. Analysis using multivariate auto‐regressive models showed that responses to environmental and ecological factors varied depending on the haplotype, which may have contributed to successful colonisation of the lake by the different haplotypes. The present results suggest that an obligate parthenogenetic population can establish in a new habitat and be maintained for generations even though it has limited genetic diversity. We found that two independent lineages (JPN1 and JPN2) successfully established and coexisted toward the end of the study period. Although limited genetic diversity did not impede colonisation success, how the later colonising JPN1 lineage has successfully invaded a population consisting solely of the early colonising JPN2 deserves future attention to understand the population genetic dynamics revealed in this study.

To lose is to win: Long‐term co‐occurrence of two asexual populations realized by a dormant strategy of the inferior competitor

“…Genetically isolated genotypes of Daphnia cf. pulex sensu Hebert (1995) are often found in single lakes (Crease et al., 1989; Hebert & Crease, 1980, 1983; Otake et al., 2022; So et al., 2015). Hebert and Crease (1980) questioned whether the co‐occurrence of obligate asexual genotypes is long‐lasting and, if so, how such a paradoxical situation is maintained.…”

“…Previous studies have shown that multiple genotypes of asexual D. cf. pulex are often found in single lakes (Otake et al, 2022;So et al, 2015). Such lakes provide an excellent opportunity to determine whether these different asexual genotypes can coexist over long periods of time, and what mechanisms enable long-term coexistence.…”

Different photoperiodic responses in diapause induction can promote the maintenance of genetic diversity via the storage effect in Daphnia pulex

“…By extending the model to incorporate spatial dynamics, it may be possible to examine whether the intraspecific difference in diapausing strategy can affect migration and range expansion. In Lake Fukami-ike, paleolimnological and population genetic analyses of diapausing eggs revealed that Jpn2C was established earlier than Jpn1A-C2T2 [ 45 ]. Further evolutionary and genetic research can contribute to our understanding of evolutionary dynamics with intraspecific interaction and spatial competition–colonization trade-off [ 81 ].…”

“…These clones were identified genetically based on mitochondrial markers in ND5 with primers ND5 f21 and ND5 r1046 [41] and the control region of mitochondrial DNA with primers IAIT fw and IAIT rv1 [41,47]. Full details of these genetic identification processes are described in our previous study [45]. We used seven clones of each genotype, Jpn1-C2T2 and Jpn2C; thus, we used 14 clones in total.…”

“…Since then, these genotypes, belonging to different lineages, coexisted for about three years in the lake. However, it seems that they went extinct around 2016 probably due to an increase in planktivorous invasive fish [ 45 ]. Here we focused on Jpn1A-C2T2 and Jpn2C, which are the dominant genotypes in the JPN1 and JPN2 lineages, respectively, and asked whether these genotypes stably coexisted and if so, what mechanisms would promote their longer coexistence.…”