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.