1. Introduction
Patterns and processes of speciation in freshwater environments are
considered to be shaped by the relatively short persistence and high
turnover rate of these habitats. Their ephemeral nature poses challenges
related to the need to seek refuge during unfavourable conditions (e.g.
drying or freezing habitats) often resulting in life history favouring
stages of dormancy, high dispersal ability, rapid population
establishment, and other r-selected traits. Moreover, the connectivity
of freshwater systems across large spatial scales, which links
ecologically distinct ecosystems (lentic and lotic), offers not only
long corridors of dispersal but also distinct selection regimes and
potential for habitat transitions.
Planktonic organisms such as Daphnia (Crustacea, Anomopoda) have
offered important insights into the evolutionary forces promoting
diversification in freshwater habitats. The biogeography of cladocerans
has been investigated for more than a century (Lampert, 2011) with the
genus Daphnia O. F. Müller, 1785 (Anomopoda: Daphniidae)
receiving particular attention. Historically, daphniids, like many
aquatic organisms, have been considered dispersalist par
excellence (Mayr, 1963) with great ability to colonize new geographic
locations and maintaining genetic cohesion across vast geographic ranges
(Bilton, Freeland, & Okamura, 2001; Bohonak & Jenkins, 2003; Havel &
Shurin, 2004). This view has been inspired by the massive production of
resting eggs which offers passive dispersal ability in both time and
space (Bilton et al., 2001). Daphniids’ resting eggs are encapsulated in
a hard structure known as an ephippium, which offers mechanical
protection and resistance to desiccation and freezing along with great
buoyancy. Ephippia enable movement between sites via vectors (e.g. water
currents, wind, animals) as well as dispersal through time via
deposition in sediments and subsequent hatching (Geerts et al., 2015;
Frisch et al., 2020). The dormant embryos encapsulated in the ephippia
can remain dormant in undisturbed sediments for decades or centuries,
forming rich ephippial banks that are considered equivalent to the seed
banks of plants (Fryer, 1996; Cáceres, 1998).
Since direct methods of measuring dispersal rates are often difficult
(Bilton et al., 2001), the high dispersal capability of daphniids (and
cladocerans in general) was inferred from observations on the viability
of ephippia after passing through the digestive tracts of animals
(Proctor & Malone, 1965; Proctor, Malone, & DeVlaming, 1967;
Figuerola, Green, & Michot, 2005), the high colonization rates of newly
created habitats, and their broad geographic distribution. Such
propensity for dispersal and long-distance colonization was assumed to
fuel high levels of gene flow and provide genetic cohesion among
populations not only at a regional scale, but also at continental and
even intercontinental scale (Mayr, 1963). The early view that
‘everything is everywhere’ was reinforced by the observed morphological
stasis (Frey, 1982; Frey, 1987) but remained untested for almost a
century.
In contrast to the traditional view of cosmopolitanism, early genetic
studies on Daphnia revealed unexpectedly high level of genetic
structure across regional and local scales (Crease, Lynch, & Spitze,
1990; Colbourne & Hebert, 1996; Schwenk et al., 1998) and high level of
cryptic endemism (Taylor, Finston, & Hebert, 1998). For example,
phylogenetic analyses of the Daphnia pulex species complex show a
polyphyletic origin of the group with European and North AmericanD. pulex diverging over 5 Mya and having distinct evolutionary
histories (Colbourne et al., 1998; Crease, Omilian, Costanzo, & Taylor,
2012; Markova, Dufresne, Manca, & Kotlik, 2013) as well as endemism
within continents. Moreover, within North America, Daphnia pulexappears to be genetically highly subdivided (Lynch & Spitze, 1994;
Crease et al., 1990). This low level of realized gene flow despite the
high potential for dispersal suggested relatively low establishment
success of new migrants. Rapid colonization, local adaptation, resting
egg banks, along with resource exploitation are believed to reduce
establishment success and gene flow among populations (De Meester,
Gomez, Okamura, & Schwenk, 2002). These observations inspired a wave of
molecular and experimental studies of the major species complexes ofDaphnia . Despite the surge in molecular ecological research
within this highly diverse genus, reproductive isolating barriers remain
poorly understood. This highlights the need for this review, which
integrates Daphnia in the framework of current speciation theory.
In this review, we explore patterns and processes of speciation in the
genus Daphnia . We searched the literature using the Web of
Science and ~30 combinations of keywords (Table 1;
Supplementary Text; Supplementary Figure 1). We first evaluate the role
of geographic barriers in restricting gene flow, and their effectiveness
in maintaining species boundaries within the genus Daphnia . We
then examine the role of ecological and nonecological isolating barriers
in restricting gene flow between closely related species (Figure 1). We
also estimate reproductive isolation metrics using methods from Sobel
and Chen (2014) based on available studies that examine reproductive
isolating barriers between closely related species of Daphnia(Table 2; Supplementary Table 1). We discuss the evolutionary forces
that promote speciation within this genus and highlight the gaps in
knowledge by exploring possible avenues of future research.