2.2.4. Postzygotic isolation
Postzygotic isolation occurs when hybridization between closely related species produces unfit hybrids due to intrinsic (developmental) or extrinsic (environmental) factors. In the Daphnia genus, interspecific hybridization is common, with closely related species in all species complexes producing hybrids with one potential exception, the Daphnia longiremis species complex. Interspecific hybridization was long suspected to occur due to the presence of intermediate morphological forms (Einsle, 1966; Lieder, 1983; Flossner & Kraus, 1986; Taylor & Hebert, 1992; Giessler, Mader, & Schwenk, 1999) and this observation was validated by molecular analyses (Wolf & Mort, 1986; Wolf, 1987; Taylor & Hebert, 1993; Spaak, 1996; Spaak, 1997; Giessler, 1997; Giessler & Englebrecht, 2009). Detailed studies on hybrids revealed intermediate life history attributes (Weider & Wolf, 1991; Spaak & Hoekstra, 1995; Dudycha & Tessier, 1999), differences in resource utilization (Boersma & Vijverberg, 1994a; Repka, 1996; Von Elert, 2004) and other ecological requirements (Taylor & Hebert, 1992; Duffy et al., 2004). Here, we summarize the potential of postzygotic isolating barriers in Daphnia based on intrinsic and extrinsic postzygotic isolation.
Intrinsic postzygotic isolation occurs as a result of genetic differences between closely related species that diminish the production and/or performance of hybrids and can occur either during the developmental process (hybrid inviability), or during sexual maturity (hybrid sterility). Three closely related species, D. galeata ,D. longispina (hyalina morph), and D. cucullata are found to co-occur in the same area or habitats, and hybridization between these three species is often bidirectional (Giessler et al., 1999). Introgression of alleles from one species to another via hybridization and backcrossing has also been documented in many studies (Taylor & Hebert, 1992; Taylor & Hebert, 1993; Schierwater, Ender, Schwenk, Spaak, & Streit, 1994; Spaak, 1996; Spaak, 1997; Spaak, Denk, Boersma, & Weider, 2004; Yin, Wolinska, & Giessler, 2010). Field experiments found low hatching success and survivorship of hybrids compared to parental species (Carvalho & Wolf, 1989; Wolf & Carvalho, 1989; Keller & Spaak, 2004; Griebel, Giessler, Yin, & Wolinska, 2016). Laboratory hatching experiments between D. galeata and D. cucullata, and D. galeata and D. longispina(hyalina morph) corroborate these findings (Schwenk, Bijl, & Menken, 2001; Keller & Spaak, 2004; Brede, Straile, Streit, & Schwenk, 2007; Keller, Wolinska, Tellenbach, & Spaak, 2007). Asymmetric reproductive isolating barriers are also observed. For example, crosses between D. cucullata females and D. galeata males are more successful than the reciprocal crosses, consistent with observations of these particular hybrids commonly found in nature (Schwenk et al., 2001). While unidirectional crosses between D. pulex females withD. pulicaria males show higher hatching and survivorship than parentals (Heier & Dudycha, 2009), postzygotic isolating barriers were found to be symmetric between D. pulex and D. pulicaria(Chin et al., 2019).
Extrinsic postzygotic isolation occurs due to ecological or behavioural differences between closely related species, which reduces the performance of hybrids that often have intermediate characteristics. In nature, hybrids are locally produced and occur in hybrid zones with environmentally favourable conditions (Taylor & Hebert, 1992; Muller & Seitz, 1995; Spaak, 1994; Spaak, 1997). Persistence of hybrids in the environment may be consistent with the hybrid inferiority model, where hybrids occur in ‘tension zones’ and experience the balancing forces of dispersal and selection against hybrids (Barton & Hewitt, 1985). However, since Daphnia hybrids can propagate by clonal reproduction, hybrid persistence and dominance can be observed in ‘tension zones’ (Weider, 1993; Spaak & Hoekstra, 1997; Schwenk, 1997), leading to the temporal hybrid superiority model (Spaak & Hoekstra, 1995). Examples of temporal hybrid superiority are relatively common inDaphnia , where hybrids are found to exhibit higher fitness than the parental species in certain environmental conditions and periods of the year, such as food quality (Seidendorf, Boersma, & Schwenk, 2007; Brzezinski & Von Elert, 2007; Weider, Jeyasingh, & Looper, 2008) and concentration (Boersma & Vijverberg, 1994b; Repka, Vesela, Weber, & Schwenk, 1999), predation (Declerck & De Meester, 2003), temperature (Weider & Wolf, 1991), parasitism (Wolinska, Bittner, Ebert, & Spaak, 2006) and a variety of other environmental factors (Griebel et al., 2015). However, hybrid fitness often varies in different environments (Loffler, Wolinska, Keeler, Rothhaupt, & Spaak, 2004). Ecological inviability of hybrids has been hypothesized to occur between hybrids ofD. cucullata and D. longispina (hyalina morph), where hybrids often occur in intermediate habitats compared to parentals (Seda, Petrusek, Machacek, & Smilauer, 2007; Petrusek et al., 2008), exhibit intermediate traits for foraging (Machacek & Seda, 2016), and lower fitness in response to predation pressure (Spaak, Vanoverbeke, & Boersma, 2000). Hybrids of D. cucullata and D. galeatadisplay intermediate traits linked to predator avoidance (Spaak, 1995). Moreover, overwintering strategies also differ between D. galeataand D. longispina (hyalina morph), where D. galeataoverwinters, D. longispina (hyalina morph) produces resting eggs, and hybrids exhibit intermediate traits (Zeis, Horn, Gigengack, Koch, & Paul, 2010). D. galeata x D. longispina (hyalina morph) hybrids are infected by parasites more often than parental species, thereby reducing their fitness (Wolinska, Keller, Bittner, Lass, & Spaak, 2004). Additionally, low fitness was observed in these hybrids under low food quality (Brzezinski, 2015).
While life history experiments to determine the role of ecology in hybrids in Daphnia are common, the potential involvement of behavioural sterility in hybrids remains largely unexplored. Detailed observations of mating behaviour of hybrids compared with parental species would greatly benefit this line of research. Experimental case studies are particularly needed to determine the extent of postzygotic isolating barriers across different sister species of Daphnia . Such studies are particularly lacking in species from the southern USA and Mexico, where endemic daphniid species inferred from allozyme data (Hebert, Schwartz, Ward, & Finston, 1993; Hebert & Finston, 1996) produce hybrids detected in intermediate habitats compared to those occupied by the parental species.