2.2.1 Ecological modes of speciation: habitat and temporal isolation
Reproductive isolating barriers could arise as a byproduct of adaption to local ecological factors (e.g. habitat preference, resource use, predation pressure) that ultimately prevent locally adapted populations from interbreeding (Coyne & Orr, 2004). Ecology can play a central role in reproductive isolation, with ecological differentiation resulting in both prezygotic and/or postzygotic isolation, to the extreme where it promotes speciation (e.g. ecological speciation, Schluter, 1996). In the case of recently diverged species that occur in distinct habitats, ecological barriers are often considered important during the early stages of speciation (Orr & Smith, 1998; Ramsey et al., 2003; Sanchez-Guillen et al., 2014). In this section, we examine the role of ecology in prezygotic isolating barriers, specifically habitat and temporal isolation as it pertains to Daphnia .
Habitat isolation occurs when potentially interbreeding species are not encountering each other during mating season due to their inability to efficiently use each other’s habitat. In the case of Daphnia , many sister species appear to inhabit various types of freshwater habitats with distinct ecology (Taylor et al., 1996; Weider et al., 1999a), such as stratified lakes with fish or ephemeral ponds with invertebrate predators. Habitat shifts have been shown to accelerate rates of evolution in Daphnia (Colbourne, Wilson, & Hebert, 2006), shape life history traits (De Mott & Pape, 2005; Seidendorf et al., 2010), morphological traits (Zellmer, 1995; Miner et al., 2013; Brandon & Dudycha, 2014), biological functions such as energy metabolism (Simcic & Brancelj, 1997; Dolling et al., 2016), and behaviours (De Meester, 1993; Pijanowska & Kowalczewski, 1997). In theD. pulex complex, the North American D. pulex inhabits ephemeral ponds, while D. pulicaria occurs in permanent lakes. There are differences in life history between them (Dudycha & Tessier, 1999; Dudycha, 2004), such as distinct anti-predator behaviour, and there is strong genetic differentiation according to habitat (Pfrender, Spitze, & Lehman, 2000). The two closely related species, D. parvula and D. retrocurva also occur in different habitats and rarely co-occur (Costanzo & Taylor, 2010). While D. parvulaoccurs in small lakes with a lower risk of invertebrate predation, and displays no morphological defenses, D. retrocurva occurs in larger habitats with a higher risk of invertebrate predation and exhibits prominent helmets as an anti-predatory defense (Beaton & Hebert, 1997).
Coexistence of closely related species in lakes is also possible due to habitat segregation and partitioning, where closely related species can be found in distinct regions of the water column (Weider, 1984), and exhibit differences in body size depending on predation risk (Leibold & Tessier, 1991; Gonzalez & Tessier, 1997; Boersma, Spaak, & De Meester, 1998) and competition for resources (Leibold, 1991; Geedy, Tessier, & Machledt, 1996). For example, although D. mendotae and D. dentifera frequently co-occur in large lakes, they segregate due to biotic factors. D. mendotae is often found in the upper water column and is better equipped to deal with invertebrate predators due to anti-predator defenses compared to D. dentifera, which inhabits the lower water column to avoid predation by fish (Taylor & Hebert, 1993; Duffy, Tessier, & Kosnik, 2004). Similarly, in the Daphnia longispina species complex, D. galeata , D. longispina(hyalina morph), and D. cucullata co-occur in the same lakes in Germany. D. longispina (hyalina morph) exhibits vertical diel migration during the year, while D. galeata remains in the upper 20m of the water column all year round (Weider & Stich, 1992). Coexistence between D. galeata and D. cucullata is possible due to niche segregation of resources due to differences in mesh size (Boersma, 1995). However, recent studies show D. galeata occurring south of the Alps at low altitudes prefer higher temperatures and higher phosphorus content (Yin, Giessler, Griebel, & Wolinska, 2014), while D. longispina (hyalina morph) andD. cucullata are distributed in the north, particularly withD. longispina (hyalina morph) occurring in large lakes with low phosphorus content (Keller, Wolinska, Manca, & Spaak, 2008). Despite habitat co-occurrence, the differential niche preferences of these two species could restrict gene flow between them. While collectively these examples suggest that habitat might play an important role in structuring species distribution in Daphnia , few experimental studies have investigated the role of ecological speciation in driving the diversification of daphniids. Furthermore, habitat choice and reciprocal transplant experiments have not been utilized to study directly the impact of habitat isolation in Daphnia speciation. However, indirect evidence for the role of habitat isolation in maintaining the integrity of species comes from studies that show how environmental stressors that impact the quality of the habitat (pollutants, metals, contaminants, temperature, etc.) can facilitate hybridization and introgression between closely related species and alter species distributions (Brede et al., 2009; Rogalski, Leavitt, & Skelly, 2017; Millette, Gonzalez, & Cristescu, 2020). Of particular interest are the genes that may be associated with habitat preference. For example, the ecological species D. pulex and D. pulicaria are fixed for different LDHA alleles, which could indicate adaptation to the different habitats due to differences in metabolic requirements in the environment (Hebert, Beaton, Schwartz, & Stanton, 1989; Crease, Floyd, Cristescu, & Innes, 2011; Cristescu, Demiri, Altshuler, & Crease, 2014).
Temporal (allochronic) isolation could also be an important barrier to gene flow in Daphnia . Closely related species often co-occur in the same habitats or region but breed (invest in sexual reproduction) at different times of the year. In the D. longispina species complex, D. galeata , D. longispina (hyalina morph) and D. cucullata are found to co-occur in lakes but sexual reproduction occurs in the spring and summer for D. galeata(Machacek, Vanickova, Seda, Cordellier, & Schwenk, 2013), whereasD. longispina (hyalina morph) and D. cucullata are found to invest in sexual reproduction during the fall season (Spaak, 1995; Spaak, 1996; Jankowski & Straile, 2004). Although strong seasonal dichotomy in sexual reproduction has not been observed between D. longispina (hyalina morph) and D. cucullata , differences in the annual occurrence of sexual reproduction between the two species has been reported (Vijverberg & Richter, 1982). In the D. pulexspecies complex, D. pulex and D. pulicaria show distinct responses to photoperiod. In laboratory conditions, the lake speciesD. pulicaria reproduces sexually during short days (Stross & Hill, 1965; Perez-Martinez, Barea-Arco, Conde-Porcuna, & Morales-Baquero, 2007) while the pond species D. pulex invests in sexual reproduction during long days (Deng, 1996; Deng, 1997). This finding reflects natural conditions, since ephemeral pond habitats are often subjected to complete evaporation by mid-summer while permanent lake habitats remain habitable until the beginning of winter (Threlkeld, 1987).
In daphniids, sex determination and sexual reproduction depend on environmental factors (Deng, 1996; Alekseev & Lampert, 2001; Tessier & Cáceres, 2004; Slusarczyk, Ochocka, & Cichocka, 2012; see Glossary). Induction of sexual reproduction of females and production of males under laboratory conditions is influenced primarily by photoperiod (Stross & Hill, 1965; Kleiven, Larsson, & Hobæk, 1992), and at times by a second stimulus such as population density (Stross & Hill, 1965; Hobæk & Larsson, 1990), temperature (Stross, 1969; Korpelainen, 1986; Camp, Haeba, & LeBlanc, 2019), chemical cues (Slusarczyk, 1995; Pijanowska & Stolpe, 1996; Navis, Waterkeyn, De Meester, & Brendonck, 2018), or a combination of these factors (Kleiven et al., 1992). Current research progress into the genetic and molecular basis of sexual reproduction revealed candidate genes that are likely to facilitate the switch from parthenogenetic reproduction to sexual reproduction (Kato et al., 2008; Liu et al., 2014; Guo et al., 2015; Li et al., 2016), including the production of ephippial eggs and males (Kato, Kobayashi, Watanabe, & Iguchi, 2011; Xu et al., 2014; Guo et al., 2015). The use of juvenile hormones such as methyl farnesoate can stimulate the production of males. Methyl farnesoate receptors trigger a signalling cascade into the downstream expression of genes that are responsible for male production (LeBlanc & Medlock, 2015; Toyota et al., 2015; Toyota, Sato, Tatarazako, & Iguchi, 2017; Camp et al., 2019), and stimulated by photoperiod and environmental cues. Moreover, recent molecular studies show that in D. magna , the switch between parthenogenetic to sexual reproduction is associated with a photoreceptor gene, rhodopsin (Roulin, Bourgeois, Stiefel, Walser, & Ebert, 2016, Toyota et al., 2019), which could be a candidate gene associated with temporal isolation between closely related species. Other candidate genes such as the temporal clock genes (per ), which have been found in theD. pulex genome (Bernatowicz et al., 2016) are likely influenced by photoperiod (Toyota et al., 2019). However, it is not clear whether there are differences in transcription activation of per across different species of Daphnia .