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 .