Abstract
Two ecological forms of the threespine stickleback Gasterosteus aculeatus – a strictly marine form and an anadromous form – are often merged in the literature as a single “marine” form. Because we know virtually nothing of the life style of the two oceanic ecotypes in the sea and consequently nothing on reproductive isolation and gene flow I argue for a precise use of the ecological terms “marine” and “anadromous” for these two ecotypes. These terms should be self-describing. The frequent use of terms incorrectly describing intraspecific variation and life style of ecotypes can bias studies on community composition and interactions of populations.
Introduction
The threespine stickleback Gasterosteus aculeatus Linnaeus, 1758 is a rare case where an ancestral marine form possibly has coexisted with its derived forms over the past million years (Wootton 1976, 1984; Bell and Foster 1994; Baker et al. 2015), or where “the ancestral condition” is represented by a “present-day oceanic stickleback” (Baker et al. 2015). Additionally, this teleost is phenotypically and ecologically extremely plastic (Wootton 1976, 1984; Bell and Foster 1994). Besides several morphological forms, three major ecological forms are discerned: two oceanic types, a strictly marine ecotype that spends its entire life cycle in a marine environment, and an anadromous ecotype that migrates as juvenile from freshwater to saltwater and returns as adult to freshwater for spawning. The third, a strictly freshwater ecotype, spends its entire life cycle in freshwater (Wootton 2009; Bell et al. 2004). The high phenotypic and ecological plasticity and an ancestral form coexisting with extant forms makes the threespine stickleback an excellent model species (Schluter 1993; McKinnon and Rundle 2002) and a species that has generated an innumerable number of publications (Wootton 2009).
The eighteenth century saw the start of an objective and scientific approach to nature and the creation of many scientific terms widely used today: e.g., “Stammzelle” (stem cell) (Haeckel 1868), “Biosphäre” (biosphere) (Suess 1875) … and “anadromous” (Myers 1949). “Anadromous” was introduced for “fishes which spend most of their lives in the sea and migrate to fresh water to breed” (Myers 1949). Like many salmonids, the threespine stickleback is a partially migratory species, viz., the species are split into migratory (anadromous) and resident populations (Jonsson and Jonsson 2009). Nevertheless, within these species the threespine stickleback is unique in splitting not only into two, but into three forms: a strictly marine, a migrating anadromous, and a strictly freshwater form. If applied, I found no case in the literature where the term “anadromous” was used inappropriately. The problem was “if applied”. In a large number of studies, the term “marine” was used instead of the correct “anadromous” or both terms were used optionally (Online Resource 1: Table S1).
Many species developed distinct phenotypes along ecological gradients which result in discrete ecotypes (e.g. Schluter and McPhail 1992; Rogers and Bernatchez 2007; Seehausen and Wagner 2014; Ahnelt et al. 2015) and differentiation in discrete ecotypes as result of selection can lead to genetic modifications and finally influences evolution (West-Eberhard 1989). Some phenotypes have split in sympatric populations (“species pairs”), e.g. freshwater threespine sticklebacks in populations inhabiting the pelagic and benthic zone of a lake respectively (Schluter and McPhail 1992; Conte and Schluter 2012). These populations represent two discrete ecotypes so called “limnetics” (plankton feeders) and “benthics” (lake bed feeders) (e.g. McKinnon and Rundle 2002; Baker et al. 2015; Vines and Schluter 2006). Although gene flow between most of these sympatric populations persisted (Schluter 1996) these two ecological terms are used frequently in recent literature (Saint-Laurent et al. 2003; Vines and Schluter 2006; Kozak et al. 2011; Jones et al. 2012) characterizing ecologically (and morphologically) divergent populations. Therefore precise use of ecological terms e.g. for the marine spawning and anadromous ecotypes of the threespine stickleback is needed.
Methods
I reviewed 109 studies published between 2000 to June 2017 for the use of ecological terms applied to the oceanic type (marine plus anadromous) of the threespine stickleback (Online Resource 1: Table S1). [Actually, there were many more publications, but I avoided repeated citing of authors who used the same name for an ecotype in subsequent studies]. In these studies I compared sampling sites with ecotypes mentioned, e.g. “marine” threespine sticklebacks sampled in a river (actually anadromous sticklebacks) to distinguish following five categories: (i) marine was conveniently or incorrectly used instead of anadromous, (ii) anadromous was correctly used for migrating sticklebacks, (iii) marine was correctly used for strictly marine sticklebacks, (iv) marine was used for sticklebacks sampled in the sea but not checked for the ecotype (anadromous or marine or a mix of both), and (v) oceanic was used to unite anadromous and marine sticklebacks.
Results
Only in 9.2% (n = 10) of the studies was the term “marine” correctly applied. This number increased to 10% if I excluded those publications in which only the term anadromous was used (n = 9) (Online Resource 1: Table S1). In nearly two-thirds of the studies (n = 69, 63.3%), the term “marine” was used instead of “anadromous”, or both terms were used optional (Fig. 1, Online Resource 1: Table S1). In the remaining studies (<30%), “anadromous” and/or “oceanic” was applied.
Discussion
The unusually high number of an inexact use of terms characterizing the life style of fish populations was surprising. A reason why “marine” is so often used instead of the correct term “anadromous” may simply be that relevant information on the lifestyle of the marine and of the anadromous ecotypes in the ocean is lacking (Bell et al. 2004; Barrett et al. 2008; Seehausen and Wagner 2014). Actually, the convenient use of the term “marine” is not rare in threespine stickleback literature and is repeatedly used optionally for “anadromous” (Online Resource 1: Table S1).
Why is “marine” so often used instead of “anadromous”? The question whether the strictly marine type and the anadromous type trace back to a common ancestor (Baker et al. 2015), or whether the anadromous threespine stickleback evolved from an extant marine stock has yet to be explored (MacColl 2009; Wund et al. 2012). Although sometimes mentioned (Bell et al. 2004; Barrett and Schluter 2008; Seehausen and Wagner 2014) no actual case has been documented where a strictly marine stickleback population evolved in the wild directly into a freshwater population. One reason why marine and anadromous ecotypes are merged into an “oceanic type” or a “marine type” (Bell et al. 2004; Wund et al. 2012) or why authors use “marine” for “anadromous” is possibly the low level of phenotypic variation of oceanic sticklebacks. Simply, we know virtually nothing of the life style of these two oceanic ecotypes in the sea (Walker and Bell 2000; Bell et al. 2009; MacColl 2009; Wund et al. 2012) and consequently we know nothing on reproductive isolation and gene flow.
The few studies on threespine sticklebacks inhabiting brackish waters revealed no definite results. In the Baltic Sea significant evidence for adaptive differentiation along a salinity gradient and local adaptation of threespine sticklebacks because of restricted gene flow was found (DeFaveri and Merilä 2013; Guo et al. 2015) but not in the St. Lawrence River estuary, also a huge brackish water system (McCairns and Bernatchez 2012).
Seemingly, many authors use the term “marine” to conveniently lump marine and anadromous sticklebacks together (Hendry and Taylor 2004; Berner et al. 2010; Kaeuffer et al. 2012; Rennison et al. 2016). Other authors switch in the same publication between “anadromous” and “marine” (Barrett and Schluter 2008; McKinnon and Rundle 2002), and some use both terms differently in subsequent publications (Berner et al. 2008, 2010; Dalziel et al. 2009, 2012). Only in a small number of publications was the merging of anadromous and marine ecotypes indicated by the use of the term “oceanic” instead (Bell et al. 2004; Shaw et al. 2007; Kimmel et al. 2012) (Online Resource 1: Table S1).
Why does it matter: Because we know virtually nothing of the life style of the two oceanic ecotypes in the sea (MacColl 2009; Wund et al. 2012). Why do some sticklebacks breed in the sea and others in fresh waters? Just by chance or are brackish environments the link between both ecotypes? We know nothing on reproductive isolation and gene flow and nothing on morphological divergence of these sticklebacks in the wild. We currently can be certain of studying marine threespine sticklebacks only if the samples were collected or observed at their oceanic spawning sites (Wund et al. 2012). The anadromous ecotype spends most of its lifetime in the sea. Thus, sampling of threespine sticklebacks in the ocean (Barber 2003; Kristjansson 2005; Marchinko 2009; Schade et al. 2014) is not a guarantee of having sampled a strictly marine stickleback. Therefore, “marine” should only be used where the specimens were observed or sampled at a marine spawning site (Bell and Peeke 2012; Demchuk et al. 2015), i.e. both terms should be self-describing. If this is not the case I suggest using the neutral term “oceanic”, which combines strictly marine and anadromous ecotypes of threespine sticklebacks (Shaw et al. 2007; Baker et al. 2008; Furin et al. 2012) at least as long as it is demonstrated that a differentiation in these two ecotypes is not justified. The frequent use of terms incorrectly describing intraspecific variation and life style of ecotypes can bias studies on community composition and interactions of populations.
References
Ahnelt H, Keckeis H, Mwebaza-Ndawula L (2015) Rapid phenotypic divergence in the small African cyprinid Rastrineobola argentea (Pellegrin 1904) (Teleostei: Cyprinidae) in Lake Victoria, Uganda. Afr J Ecol 54:107–110. https://doi.org/10.1111/aje.12236
Baker JA, Heins DC, Foster SA, King RW (2008) An overview of life-history variation in female threespine stickleback. Behaviour 145:579–602. https://doi.org/10.1163/156853908792451539
Baker JA, Wund MA, Heins DC, King RW, Foster SA (2015) Life-history plasticity in female threespine stickleback. Heredity 115:322–334. https://doi.org/10.1038/hdy.2015.65
Barber I (2003) Parasites and size-assortative schooling in three-spined sticklebacks. Oikos 101:331–337
Barrett DJ (2010) Adaptive evolution of lateral plates in three-spined stickleback Gasterosteus aculeatus: a case study in functional analysis of natural variation. J Fish Biol 77:311–328. https://doi.org/10.1111/j.1095-8649.2010.02640.x
Barrett RDH, Schluter D (2008) Adaptation from standing genetic variation. Trends Ecol Evol 23:38–44. https://doi.org/10.1016/j.tree.2007.09.008
Barrett RD, Rogers SM, Schluter D (2008) Natural selection on a major armor gene in threespine stickleback. Science 322:255–257. https://doi.org/10.1126/science.1159978
Bell MA, Foster SA (1994) The evolutionary biology of the threespine stickleback. Oxford University Press
Bell AM, Peeke HVS (2012) Individual variation in habituation: behavior over time toward different stimuli in threespine sticklebacks (Gasterosteus aculeatus). Behaviour 149:1339–1365. https://doi.org/10.1163/1568539X-00003019
Bell MA, Aguirre WE, Buck NJ (2004) Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58:814–824. https://doi.org/10.1111/j.0014-3820.2004.tb00414.x
Bell MA, Stewart JD, Parker PJ (2009) The world’s oldest fossil threespine stickleback fish. Copeia 2009:256–265. https://doi.org/10.1643/CG-08-059
Berner D, Adams DC, Grandchmp A-C, Hendry AP (2008) Natural selection drives patterns of lake-stream divergence in stickleback foraging strategy. J Evol Biol 21:1653–1665. https://doi.org/10.1111/j.1420-9101.2008.01583.x
Conte GL, Schluter D (2012) Experimental confirmation that body size determines mate preference via phenotype matching in a stickleback species pair. Evolution 67:1477–1484. https://doi.org/10.1111/evo.12041
Dalziel AC, Rogers SM, Schulte PM (2009) Linking genotypes to phenotypes and fitness: how mechanistic biology can inform molecular ecology. Mol Ecol 18:4997–5017. https://doi.org/10.1111/j.1365-294X.2009.04427.x
Dalziel, AC, Vines TH, Dchulte PM (2012) Reductions in prolonged swimming capacity following freshwater colonization in multiple threespine stickleback populations. Evolution 66:1226–1239. https://doi.org/10.1111/j.1558-5646.2011.0149.x
DeFaveri J, Merilä J (2013) Heterogenous genomic differentiation in marine threespine sticklebacks: adaption along an environmental gradient. Evolution 67:2530–2546. https://doi.org/10.1111/evo.12097
Demchuk A, Ivanov M, Polyalova N, Mas-Marití E, Lajus A (2015) Feeding patterns in seagrass beds of three-spined stickleback Gasterosteus aculeatus juveniles at different growth stages. J Mar Biol Assoc UK 95:1–9. https://doi.org/10.1017/S0025315415000569
Furin CG, von Hippel FA, Bell MA (2012) Partial reproductive isolation of a recently derived resident-freshwater population of threespine stickleback (Gasterosteus aculeatus) from its putative anadromous ancestor. Evolution 66:3277–3286. https://doi.org/10.1111/j.1558-5646.2012.01672.x
Guo B, DeFaveri J, Sotelo G, Nair A, Merilä J (2015) Population genomic evidence for adaptive differentiation in Baltic three-spined sticklebacks. BMC Biol 13:19. https://doi.org/10.1186/s12915-015-0130-8
Haeckel E (1868) Natürliche Schöpfungsgeschichte. Gemeinverständliche wissenschaftliche Vorträge über die Entwicklungs-Lehre im Allgemeinen und diejenigen von Darwin. Goethe und Lamarck, Georg Reimer, Berlin
Hendry AP, Taylor EB (2004) How much of the variation in adaptive divergence can be explained by gene flow? An evaluation using lake-stream stickleback pairs. Evolution 58:2319–2331. https://doi.org/10.1111/j.0014-3820.2004.tb01606.x
Jones FC, Grabherr MG, Chan YF et al (2012) The genomic basis of adaptive evolution in threespine stickleback. Nature 484:55–61. https://doi.org/10.1038/nature10944
Jonsson B, Jonsson NJ (2009) A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta, with particular reference to water temperature and flow. Fish Biol 75:2381–2447. https://doi.org/10.1111/j.1095-8649.2009.02380.x
Kaeuffer R, Peichel CL, Bolnick DI, Hendry AP (2012) Parallel and nonparallel aspects of ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback. Evolution 66:402–418. https://doi.org/10.1111/j.1558-5646.2011.01440.x
Kimmel CB, Ullmann B, Currey M, Hohenlohe PA, Cresko WA (2012) Developmental dissociation in morphological evolution of the stickleback opercle. Evolution 66:419–434. https://doi.org/10.1111/j.1525-142X.2012.00551.x
Kozak M, Head ML, Boughman JW (2011) Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks. Proc R Soc B 278:2604–2610. https://doi.org/10.1098/rspb.2010.2466
Kristjansson BK (2005) Rapid morphological changes in threespine stickleback, Gasterosteus aculeatus, in freshwater. Env Biol Fishes 74:357–363. https://doi.org/10.1242/jeb.00994
MacColl ADC (2009) Parasites may contribute to ‘magic trait’ evolution in the adaptive radiation of three-spined sticklebacks, Gasterosteus aculeatus (Gasterosteiformes: Gasterosteidae). Biol J Linn Soc 96:425–433. https://doi.org/10.1111/j.1095-8312.2008.01123.x
Marchinko KB (2009) Predation’s role in repeated phenotypic and genetic divergence of armor in threespine stickleback. Evolution 63:127–138. https://doi.org/10.1111/j.1558-5646.2008.00529.x
McCairns RJS, Bernatchez J (2012) Plasticity and herability of morphological variation within an between parapatric stickleback deems. J Evol Biol 25:1097–1112. https://doi.org/10.1111/j.1420-9101.2012.02496.x
McKinnon JS, Rundle HD (2002) Speciation in nature: the threespine stickleback model systems. Trends Ecol Evol 17:480–488
Myers GS (1949) Usage of anadromous, catadromous and allied terms for migratory fish. Copeia 1949:89–96
Rennison DJ, Owens GL, Heckman N, Schluter D, Veen T (2016) Rapid adaptive evolution of colour vision in the threespine stickleback radiation. Proc Biol Soc B 2 283:20160242. https://doi.org/10.1098/rspb.2016.0242
Rogers SM, Bernatchez L (2007) The gene architecture of ecological speciation and the association with signatures of selektion in natural lake whitefish (Coregonus sp. Salmonidae) species pairs. Mol Biol Evol 24:1423–1148. https://doi.org/10.1093/molbev/msm066
Saint-Laurent R, Legault M, Bernatchez L (2003) Divergent selection maintains adaptive differentiation despite high gene flow between sympatric rainbow smelt ecotypes (Osmerus mordax Mitchill). Mol Ecol 12(2):315–330
Schade FM, Clemmesen C, Wegner KM (2014) Within and transgenerational effects of ocean acidification on life history of marine three-spined stickleback (Gasterosteus aculeatus). Mar Biol 161:1667–1676. https://doi.org/10.1007/s00227-014-2450-6
Schluter D (1993) Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology 74:699–709
Schluter D (1996) Adaptive radiation along genetic lines of least resistance. Evolution 50:1766–1774
Schluter D, McPhail JD (1992) Ecological character displacement and speciation in sticklenbacks. Am Nat 140:85–108
Seehausen O, Wagner CE (2014) Speciation in freshwater fishes. Ann Rev Ecol Evol Syst 45:621–651. https://doi.org/10.1146/annurev-ecolsys-120213-091818
Shaw KA, Scott LM, Foster SA (2007) Ancestral plasticity and the evolutionary diversification of courtship behaviour in threespine stickleback. Anim Behav 73:415–422. https://doi.org/10.1016/j.anbehav.2006.09.002
Suess E (1875) Die Entstehung der Alpen. Wilhelm Braumüller, Wien
Vines TH, Schluter D (2006) Strong assortative mating between allopatric sticklebacks as a by-product of adaptation to different environments. Proc Biol Sci B 273:911–916. https://doi.org/10.1098/rspb.2005.3387
Walker JA, Bell MA (2000) Net evolutionary trajectories of body shape evolution within a microgeographic radiationof threespine sticklebacks (Gasterosteus aculeatus). J Zool 252:293–302. https://doi.org/10.1111/j.1469-7998.2000.tb00624.x
West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Ann Rev Ecol Syst 20:249–278
Wootton RJ (1976) The biology of the sticklebacks. Academic Press, London
Wootton RJ (1984) A functional biology of sticklebacks. University of California Press
Wootton RJ (2009) The Darwinian stickleback. Gasterosteus aculeatus: a history of evolutionary studies. J Fish Biol 75:1919–1942. https://doi.org/10.1111/j.1095-8649.2009.02412.x
Wund MA, Baker JA, Clancy B, Golub J, Foster SA (2012) A test of the “flexible stem” model of evolution: ancestral plasticity and allometry in threespine stickleback fish reveal phenotypes associated with derived, freshwater ecotypes. Biol J Linn Soc 105:573–583. https://doi.org/10.1086/59096
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Open access funding provided by University of Vienna. I thank N. Gansinger for support with the graphics and T. Iwamoto for reviewing the English.
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Ahnelt, H. Imprecise naming: the anadromous and the sea spawning threespine stickleback should be discriminated by names. Biologia 73, 389–392 (2018). https://doi.org/10.2478/s11756-018-0038-1
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DOI: https://doi.org/10.2478/s11756-018-0038-1