Review Article |
Corresponding author: David J. Wildish ( talitridnb@gmail.com ) Academic editor: Pavel Stoev
© 2020 David J. Wildish, Adriana E. Radulovici.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Wildish DJ, Radulovici AE (2020) Amphipods in estuaries: the sibling species low salinity switch hypothesis. Zoosystematics and Evolution 96(2): 797-805. https://doi.org/10.3897/zse.96.55896
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A novel low salinity switch hypothesis is proposed to account for the speciation of an obligate estuarine (oligohaline) amphipod, Orchestia aestuarensis, from a closely-related one, Orchestia mediterranea, found in both estuarine and marine conditions (euryhaline). The underlying genetic mechanisms could involve:
1. A dimorphic allele, or linked set of alleles, carried by the euryhaline amphipod which controls the ability to breed in low salinity conditions in estuaries and which is selected for in these conditions, producing the oligohaline amphipod.
2. A genetically-assimilated gene or genes, controlling the ability to breed in low salinity conditions in estuaries, which is/are “switched on” by low salinity conditions.
3. Allopatric speciation from a euryhaline to an oligohaline amphipod species where low salinity conditions is the selective switch.
It is possible that other estuarine, sibling, amphipod pairs have evolved by salinity switching. In the North Atlantic coastal region, this could include: Gammarus tigrinus/G. daiberi and G. salinus/G. zaddachi (Amphipoda, Gammaridae).
Low salinity switch hypothesis, sibling species amphipods, evolution, estuaries, O. mediterranea, O. aestuarensis
The Amphipoda are one of 16 orders of the Crustacea (Horton et al., 2016). Over nine thousand (9,980) species of amphipods have been described to 2016 (
The Amphipoda contain species which extend from the marine environment into estuaries and freshwater. In colonising estuaries, the immigrant species demonstrate varying degrees of physiological acclimatisation or adaptation to the reduced salinities, which is the defining feature of estuaries.
We review the literature pertinent to sibling species pairs in estuaries and propose the low salinity switch hypothesis to explain their evolutionary origin. Our review focuses on the euryhaline talitrid: Orchestia mediterranea A. Costa, 1853 (Crustacea, Amphipoda, Talitridae) and its oligohaline sibling, Orchestia aestuarensis, Wildish, 1987. A description of the kinds of estuaries that amphipods might encounter as they colonise them is given. Study methods are reviewed which can examine the inference that the oligohaline amphipod evolved by salinity switching from its euryhaline sibling.
An estuary is that part of the hydrological system where freshwater and marine waters mix. Classification of estuaries is based either on how they geologically form or how and where, the waters mix within them (
The classification based on how and where fresh and saltwater mix within the estuary is of most use in this study.
In this study, we have relied on direct measurement of chlorinity or salinity in the estuary, accounting for tidal effects to correlate with amphipod distribution. Up until the 1980s, salinity was measured by titrating the halide content with silver nitrate, yielding a “chlorinity” as parts per thousand (ppt), which, if multiplied by 1.80655, gives salinity as ppt. Assuming that typical, undiluted seawater has a salinity of 35g/kg or 35 ppt, the earlier chlorinity measurements can be converted to a percentage of 35 ppt salinity seawater and this is the most useful way of expressing it if salinity tolerance experiments are contemplated. From the 1980s onwards, salinity measurements were increasingly made by electrical conductivity methods and the results expressed as practical salinity units (PSU). Such measurements may be converted from the relationship: 35 PSU = 100% seawater.
The hypothesis, proposed here, is that low salinity acts as an environmental switch by “choosing” the new phenotype, which can live and reproduce at lower salinities, from amongst adjacent euryhaline, sibling populations which are adapted to live and reproduce in a higher range of salinities. Thus, the new phenotype is “induced” by the appropriate salinity conditions in a new estuary from a euryhaline, sibling population reaching the appropriate salinity conditions. Specific mechanisms which could control the appearance of an oligohaline from a euryhaline amphipod in low salinity locations in estuaries include:
The null hypothesis for each of the hypothetical mechanisms above would be that genetic change and natural selection were not involved in the phenotypic changes observed.
Orchestia mediterranea A. Costa, 1857 and O. aestuarensis Wildish, 1987 were selected, based on the following biological/geological criteria:
In what follows, we review, in the same order as listed above, the literature available for each of the six criteria as it pertains to the evolution of O. aestuarensis and O. mediterranea in estuaries.
A synonomy list for O. mediterranea is given in
O. aestuarensis was originally described as a morph of O. mediterranea and not given specific status until 1987 (
To date, the British estuaries, Tamar, Medway and Duddon are the only ones where comprehensive estuarine distribution data has been collected. Results are summarised in
Mixed species populations occur only at the interface between O. aestuarensis and O. mediterranea distribution in the Tamar Estuary. Landwards of this interface location, only O. aestuarensis occurs and seaward only O. mediterranea. This distribution is interpreted to be governed by a low salinity switch at a location in the estuary where both species can co-exist. In the Medway Estuary, O. aestuarensis is present from above the Medway bridge, up-estuary for ~2.5 km (approximately one half of the mesohalinicum). Estuarine penetration terminates in the Medway where the highwater salinity is 31% of seawater (Fig.
Morphologically, O. aestuarensis is close to O. mediterranea, although it can be distinguished by a number of minor taxonomic characters (
The hybridisation studies in the Medway Estuary suggest that reproductive isolation between the two species is incomplete. The source of the two populations used in the British hybridisation experiments were ~8 km apart along the estuarine gradient: the most landward colony sampled was in the mesohalinicum and the most seaward in the polyhalinicum (
Species of Orchestia are sensitive to salinity conditions in estuaries and in lowland estuaries the high tide salinity may represent the salinity distribution limits (Table
Distribution limits at high water of Orchestia in two lowland estuaries: Deltaic Area, The Netherlands (
Species | Deltaic Area | Medway estuary | ||
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Salinity (ppt) | Percent of full-strength seawater (S = 35ppt) | Salinity (ppt) | Percent of full-strength seawater (S = 35ppt) | |
O. gammarellus | 3.25 > 29.81 | 9.3–100 | 1.81 > 29.81 | 5.2–100 |
O. mediterranea | 9.03 > 29.81 | 25.8–100 | 18.07 > 29.81 | 51.6–100 |
O. aestuarensis | ? | ? | 10.84–18.07 | 31–51.6 |
Experiments with diluted seawater and O. mediterranea showed that lethality (lethal concentration at which 50% of those tested die, LC50) was dependent on the inter-moult stage, with a wide range of 48-hour LC50s from 2 -15% of 35 ppt seawater (
Great strides have been achieved in understanding the physiology of ionic and osmotic regulation in talitrids (
The Barcode of Life Data System (BOLD, wwwboldsystems.org,
The importance of the geological background in the study of O. mediterranea in estuaries of the coasts of the northeast Atlantic and Mediterranean Sea is that it provides a timescale for the evolution of its sibling species O. aestuarensis.
The Pleistocene history of the Thames and Medway estuaries in Britain are discussed by
None of the glacials, including the last, the Devensian (115,000 to 11,700 years BP), reached the southern estuaries (e.g. Medway, Tamar) in Britain (
All three of the proposed mechanisms of in situ evolution of O. aestuarensis from O. mediterranea in estuaries avoid the need for natural dispersal by the low salinity sibling from one estuary to another. Hypothetical mechanism 3 involves de novo evolution in each new estuary colonised by O. mediterranea. It seems to be less likely in view of the phenotypic similarities found in the few populations so far studied. The oligohaline O. aestuarensis in northern Britain would have diverged more recently (< 10,000 years) than southern species (> 400,000 years). Population divergence estimates, based on molecular genetic methods, such as the mitochondrial CO1gene (
For the ability to breed at low salinity (< 52% seawater), we propose that a dimorphic allele or linked set of alleles is selected for by low salinity conditions, a gene(s) is/are switched on by low salinity conditions or allopatric or parapatric speciation occurs in each new estuary, colonised by O. mediterranea. The minor morphological and dorsal pigment pattern differences with O. mediterranea in O. aestuarensis (
In a laboratory intrapopulation cross with males and females of O. mediterranea at Upnor Castle (polyhalinicum),
Histological observations and grafting experiments undertaken by
In an earlier paper (
The genetic changes hypothesised to underlie low salinity switching in Orchestia occurred in the geological (recent) past, likely in different environments than those of today. It is therefore problematic to use direct experimentation to test the natural selection hypothesised to be involved. Instead, we have proposed inductive inference methods to do this. Strong evidence in support of low salinity switching will be provided if all the individual criteria, zoogeographic, physiological, ecological and genetic, reviewed above, support it.
Other species of amphipods are known to be sensitive to salinity conditions and some are confined to estuaries as sibling species (e.g. some gammarids) (Table
Putative sibling species pairs of Gammaridae associated with estuaries from the North Atlantic Ocean. Taxonomic names as in World Register of Marine Species (WoRMS), accessed April 2019, CO1 data from BOLD accessed May 2020, N = number of oligohaline/euryhaline individuals.
Estuary | Putative Sibling Species Pair | Reference | Mean % COI genetic distance | N | |
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Brackish / estuarine (oligohaline) | Marin e/ Estuarine (euryhaline) | ||||
Canadian estuaries | Gammarus tigrinus Sexton, 1939 | Gammarus lawrencianus Bousfield, 1956 |
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24.86 | 172/70 |
North American estuaries | Gammarus daiberi Bousfield, 1969 | Gammarus tigrinus Sexton, 1939 |
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14.54 | 4/172 |
Deltaic Area, Holland | Gammarus zaddachi Sexton,1912 | Gammarus salinus Spooner,1947 |
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14.62 | 60/82 |
Deltaic Area, Holland | Gammarus salinus Spooner,1947 | Gammarus locusta (Linnaeus,1758) |
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26.35 | 82/94 |
Deltaic Area, Holland | Echinogammarus marinus (Leach, 1815) | Echinogammarus obtusatus (Dahl, 1938) |
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33.29 | 36/31 |
Genetic relatedness and ecological data (that the oligohaline amphipod is limited to low salinities in estuaries), together with other related biological data, are suggestive that low salinity conditions directed the evolution in these amphipods.
This study illustrates that limited ecological/genetic data are useful in identifying pairs of sibling species of estuarine amphipods which may have evolved by salinity switching. Using this method, three sibling species pairs were identified: O. aestuarensis/O. mediterranea, G. zaddachi/G. salinus and G. daiberi/G. tigrinus. Further studies, based on the six biological/geological criteria used herein to infer salinity switch evolution in O. aestuarensis/O. mediterranea, could be applied to the two selected Gammarus sp. siblings. The location of a gene(s) for salinity switching would ultimately confirm the hypothesis.
We suspect that there will be other sibling species pairs of amphipods which have evolved in this way in other estuaries throughout the world and that our study is a step forward in shedding light on estuarine amphipod evolution.
We thank Ms. Enid Bradley and Mr. John Bratton for sharing their discoveries of O. aestuarensis in the Duddon and Humber estuaries, respectively and a reviewer for improving an earlier version. Thanks to the Museum für Naturkunde, Berlin for supporting the publication costs.