Lateral Plate Morphs Research Articles

Temperature-Dependent Reproductive Success of Stickleback Lateral Plate Morphs: Implications for Population Polymorphism and Range Shifts Under Ocean Warming

Changing environments associated with rapid climate change can shape direct measures of fitness such as reproductive success by altering mating behavior, fecundity and offspring development. Using a polymorphic oceanic population of threespine stickleback (Gasterosteus aculeatus), we investigated whether a 4°C increase in sea surface temperature influenced clutch siring success, reproductive output, and offspring growth among lateral plate morphs. Since low plated morphs are thought to have a selective advantage in warmer environments, we predicted that low plated males should have higher clutch siring success in +4°C environments, and that thermal plasticity of traits (e.g., egg size, offspring growth) should reflect different trait optima in different environments among plate morphs. Parentage analysis of egg clutches revealed temperature-specific clutch siring success, in that low plated males sired more clutches in +4°C environments and completely plated males sired more clutches at ambient (seasonal) temperature. Both completely and low plated females laid larger eggs when acclimated to +4°C, but only completely plated females had smaller clutches at +4°C. Offspring of low and partially plated females grew much less at +4°C compared to those of completely plated females. Taken together, our results demonstrate that ocean warming could impact reproductive success at various levels, with differential effects depending on phenotype, in this case, lateral plate morph. Some traits (clutch siring success, egg size) showed better performance for low plated fish at +4°C, whereas others (e.g., growth) did not. Higher clutch siring success of low plated males at elevated temperature might indicate a future shift in plate morph composition for polymorphic stickleback populations, with potential implications for colonization ability during range shifts under climate change.

Allometric relationships in morphological traits associated with foraging, swimming ability, and predator defense reveal adaptations toward brackish and freshwater environments in the threespine stickleback.

Freshwater colonization by threespine stickleback has led to divergence in morphology between ancestral marine and derived freshwater populations, making them ideal for studying natural selection on phenotypes. In an open brackish–freshwater system, we previously discovered two genetically distinct stickleback populations that also differ in geometric shape: one mainly found in the brackish water lagoon and one throughout the freshwater system. As shape and size are not perfectly correlated, the aim of this study was to identify the morphological trait(s) that separated the populations in geometric shape. We measured 23 phenotypes likely to be important for foraging, swimming capacity, and defense against predation. The lateral plate morphs in freshwater displayed few significant changes in trait sizes, but the low plated expressed feeding traits more associated with benthic habitats. When comparing the completely plated genetically assigned populations, the freshwater, the hybrids, the migrants and the lagoon fish, many of the linear traits had different slopes and intercepts in trait‐size regressions, precluding our ability to directly compare all traits simultaneously, which most likely results from low variation in body length for the lagoon and migrant population. We found the lagoon stickleback population to be more specialized toward the littoral zone, displaying benthic traits such as large, deep bodies with smaller eyes compared to the freshwater completely plated morph. Further, the lagoon and migrant fish had an overall higher body coverage of lateral plates compared to freshwater fish, and the dorsal and pelvic spines were longer. Evolutionary constraints due to allometric scaling relationships could explain the observed, overall restricted, differences in morphology between the sticklebacks in this study, as most traits have diversified in common allometric trajectories. The observed differences in foraging and antipredation traits between the fish with a lagoon and freshwater genetic signature are likely a result of genetic or plastic adaptations toward brackish and freshwater environments.

Ongoing niche differentiation under high gene flow in a polymorphic brackish water threespine stickleback (Gasterosteus aculeatus) population

BackgroundMarine threespine sticklebacks colonized and adapted to brackish and freshwater environments since the last Pleistocene glacial. Throughout the Holarctic, three lateral plate morphs are observed; the low, partial and completely plated morph. We test if the three plate morphs in the brackish water Lake Engervann, Norway, differ in body size, trophic morphology (gill raker number and length), niche (stable isotopes; δ15N, δ13C, and parasites (Theristina gasterostei, Trematoda spp.)), genetic structure (microsatellites) and the lateral-plate encoding Stn382 (Ectodysplasin) gene. We examine differences temporally (autumn 2006/spring 2007) and spatially (upper/lower sections of the lake – reflecting low versus high salinity).ResultsAll morphs belonged to one gene pool. The complete morph was larger than the low plated, with the partial morph intermediate. The number of lateral plates ranged 8–71, with means of 64.2 for complete, 40.3 for partial, and 14.9 for low plated morph. Stickleback δ15N was higher in the lower lake section, while δ13C was higher in the upper section. Stickleback isotopic values were greater in autumn. The low plated morph had larger variances in δ15N and δ13C than the other morphs. Sticklebacks in the upper section had more T. gasterostei than in the lower section which had more Trematoda spp. Sticklebacks had less T. gasterostei, but more Trematoda spp. in autumn than spring. Sticklebacks with few and short rakers had more T. gasterostei, while sticklebacks with longer rakers had more Trematoda. spp. Stickleback with higher δ15N values had more T. gasterostei, while sticklebacks with higher δ15N and δ13C values had more Trematoda spp. The low plated morph had fewer Trematoda spp. than other morphs.ConclusionsTrait-ecology associations may imply that the three lateral plate morphs in the brackish water lagoon of Lake Engervann are experiencing ongoing divergent selection for niche and migratory life history strategies under high gene flow. As such, the brackish water zone may generally act as a generator of genomic diversity to be selected upon in the different environments where threespine sticklebacks can live.

Low genetic and phenotypic divergence in a contact zone between freshwater and marine sticklebacks: gene flow constrains adaptation

BackgroundDistinct hybrid zones and phenotypic and genomic divergence is often observed between marine and freshwater threespine sticklebacks (Gasterosteus aculeatus). Nevertheless, cases also exist where marine-freshwater divergence is diffuse despite seemingly similar environmental settings. In order to assess what characterizes these highly different outcomes, we focused on the latter kind of system in the Odder River, Denmark. Here, a previous study based on RAD (Restriction site Associated DNA) sequencing found non-significant genome-wide differentiation between marine and freshwater sticklebacks. In the present study, we analyzed samples on a finer geographical scale. We assessed if the system should be regarded as panmictic, or if fine-scale genetic structure and local selection was present but dominated by strong migration. We also asked if specific population components, that is the two sexes and different lateral plate morphs, contributed disproportionally more to dispersal.ResultsWe assessed variation at 96 SNPs and the Eda gene that affects lateral plate number, conducted molecular sex identification, and analyzed morphological traits. Genetic differentiation estimated by FST was non-significant throughout the system. Nevertheless, spatial autocorrelation analysis suggested fine scale genetic structure with a genetic patch size of 770 m. There was no evidence for sex-biased dispersal, but full-plated individuals showed higher dispersal than low- and partial-plated individuals. The system was dominated by full-plated morphs characteristic of marine sticklebacks, but in the upstream part of the river body shape and frequency of low-plated morphs changed in the direction expected for freshwater sticklebacks. Five markers including Eda were under possible diversifying selection. However, only subtle clinal patterns were observed for traits and markers.ConclusionsWe suggest that gene flow from marine sticklebacks overwhelms adaptation to freshwater conditions, but the short genetic patch size means that the effect of gene flow on the most upstream region must be indirect and occurs over generations. The occurrence of both weak unimodal and strong bimodal hybrid zones within the same species is striking. We suggest environmental and demographic factors that could determine these outcomes, but also highlight the possibility that long-term population history and the presence or absence of genomic incompatibilities could be a contributing factor.

The impact of selection, gene flow and demographic history on heterogeneous genomic divergence: three-spine sticklebacks in divergent environments.

Heterogeneous genomic divergence between populations may reflect selection, but should also be seen in conjunction with gene flow and drift, particularly population bottlenecks. Marine and freshwater three-spine stickleback (Gasterosteus aculeatus) populations often exhibit different lateral armour plate morphs. Moreover, strikingly parallel genomic footprints across different marine-freshwater population pairs are interpreted as parallel evolution and gene reuse. Nevertheless, in some geographic regions like the North Sea and Baltic Sea, different patterns are observed. Freshwater populations in coastal regions are often dominated by marine morphs, suggesting that gene flow overwhelms selection, and genomic parallelism may also be less pronounced. We used RAD sequencing for analysing 28 888 SNPs in two marine and seven freshwater populations in Denmark, Europe. Freshwater populations represented a variety of environments: river populations accessible to gene flow from marine sticklebacks and large and small isolated lakes with and without fish predators. Sticklebacks in an accessible river environment showed minimal morphological and genomewide divergence from marine populations, supporting the hypothesis of gene flow overriding selection. Allele frequency spectra suggested bottlenecks in all freshwater populations, and particularly two small lake populations. However, genomic footprints ascribed to selection could nevertheless be identified. No genomic regions were consistent freshwater-marine outliers, and parallelism was much lower than in other comparable studies. Two genomic regions previously described to be under divergent selection in freshwater and marine populations were outliers between different freshwater populations. We ascribe these patterns to stronger environmental heterogeneity among freshwater populations in our study as compared to most other studies, although the demographic history involving bottlenecks should also be considered in the interpretation of results.

Covariation in shape and foraging behaviour in lateral plate morphs in the three‐spined stickleback

Bjærke O, Østbye K, Lampe HM, Vøllestad LA. Covariation in shape and foraging behaviour in lateral plate morphs in the three‐spined stickleback. Ecology of Freshwater Fish 2010: 19: 249–256. © 2010 John Wiley & Sons A/SAbstract – In three‐spined stickleback (Gasterosteus aculeatus) colonisation of freshwater has led to rapid evolution in various morphological and behavioural traits. Examples are reduction in lateral plate number and increased benthic foraging. These changes are believed to result from natural selection, but the evolutionary mechanisms driving behavioural changes and how such changes are associated with phenotypes, are poorly understood. Here, we study three different lateral plate morphs from a brackish water lake and one morph from a river upstream. We investigate if the lateral plate morphs differ in overall body shape and then experimentally test how foraging behaviour differ among morphs and with body shape. Foraging behaviour is measured as the consumption efficiency of benthic and pelagic prey types. The results show that lateral plate morphs differ in overall body shape and that body shape significantly co‐varies with foraging behaviour.

PARALLEL EVOLUTION BY CORRELATED RESPONSE: LATERAL PLATE REDUCTION IN THREESPINE STICKLEBACK

Recent work has revealed the molecular mechanisms governing one of the most dramatic examples of parallel evolution in nature: the repeated loss of lateral plate armor in freshwater populations of threespine stickleback. Yet, the ecological mechanisms responsible for armor loss remain unclear. Using a balanced experimental design, we examined Heuts' (1947) hypothesis that selection due to differences in salinity indirectly drive the reduction of lateral plate armor in fresh water while maintaining armor in the sea. We measured two fitness-related traits, hatching success and juvenile growth rate, in offspring of reduced (low and partial) and complete lateral plate morphs from two polymorphic populations when raised in either fresh water or salt water. In contrast to Heuts' results, there was little difference among morphs in hatching success. However, salinity strongly influenced juvenile growth: offspring of reduced lateral plate morphs grew substantially faster (up to 65%) than offspring of completely plated morphs in fresh water, but there was little difference in salt water. We suggest that the parallel loss of lateral plates in fresh water has arisen through a correlated response to selection for faster growth during lateral plate development, but the effect of salinity on hatching success and juvenile growth rate cannot explain the predominance of completely plated morphs in marine populations.

Genetics of Lateral Plate and Gillraker Phenotypes in a Rapidly Evolving Population of Threespine Stickleback

Twenty-seven crosses were used to study the genetics of rapidly evolving traits in a recently founded population of threespine stickleback in Loberg Lake, Alaska. Lateral plate morph segregation ratios were inconsistent with all published models of lateral plate morph genetics except Avise's (1976) general two-locus model. Incompatibility of the results of our plate morph crosses with those of most previous studies suggests that the genetic architecture underlying lateral plate morphs differs among populations or is more complex than presently recognized. Segregation ratios for lateral plate morphs indicate that consistently low frequencies of partial morphs observed in the Loberg Lake population at least partly reflect genetic architecture. Gillraker number and probably low morph lateral plate number are highly heritable and correlated with each other. Lateral plate asymmetry was high but not significantly heritable. Low and complete morph lateral plate number do not appear to be genetically correlated, indicating a significant element of independent genetic control.

Lateral Plate Polymorphism in Marine and Estuarine Populations of the Threespine Stickleback (Gasterosteus aculeatus) along the Coast of Norway

Marine populations of the threespine stickleback (Gasterosteus aculeatus) have mostly been described as monomorphic for the complete lateral plate morph, especially in northern waters. An examination of stickleback populations from 27 marine and estuarine sites along the coast of Norway showed that polymorphism is more common than expected; in fact, only 15% of the samples were monomorphic. Populations from estuarine habitats (low salinity) were more polymorphic than populations from marine habitats. A study of morphometric characters shows that the plate morph variation reflects true polymorphism, not just immigration of freshwater sticklebacks or hybridization. Plate number variation within each plate morph was also recorded, but no pattern of variation could be detected, either geographically, or between estuarine and marine habitats.

Lateral Plate Morph Genetics Revisited: Evidence for a Fourth Morph in Three-Spined Sticklebacks

Abstract1. The view that four (not three) lateral plate morphs exist in the three-spined stickleback Gasterosteus aculeatus is supported in this paper. The morphs are: trachura (= completely plated), semiarmata (= partially plated), leiura (= low plated), and leiura-with-keel (= low-plated-with-keel). 2. Two one-locus and four two-locus models of lateral plate morph inheritance are identified and reviewed. A new genetic model for a two-locus system comprising one major gene with three alleles and one dominance modifier gene with two alleles is advocated. 3. Predictions of different models are explicitly examined using the existent data. 4. Results of 10 new crosses that distinguished the form leiura-with-keel are presented. The segregation ratios obtained are best explained by the new model. 5. Adaptive value of plate morph differentiation is not clear. Different aspects of selection on the morphs are discussed.

Reproductive Isolation Among Lateral Plate Phenotypes (Low, Partial, Complete) of the Threespine Stickleback, Gasterosteus Aculeatus, From the White Sea Basin and the Kamchatka Peninsula, Russia

AbstractReproductive isolation was investigated among sympatric lateral plate morphs of threespine stickleback from the White Sea basin and also among phenotypically similar morphs from the distant Kamchatka River basin (Lake Azabachije). Female choice tests show that gene flow is restricted among the completely plated and low plated morphs at both locations; behavioural isolation between these morphs is complete among Lake Azabachije fish, and nearly so (93% positive assortative mating) among White Sea basin fish. However, the experiments also demonstrate that there are no barriers to reproduction among the Azabachije and White Sea complete morphs, among the Azabachije low and White Sea complete morphs, nor among the Azabachije complete and White Sea low morphs. In addition, there is no evidence of barriers to gene flow among the low and partially plated morphs. Therefore, although gene flow is restricted among the extreme morphs within each locality, nevertheless gene exchange is possible, either directly or secondarily, among all phenotypes. The reproductive isolation between the complete and low morphs from the White Sea basin developed in situ no more than eight generations after the sticklebacks were introduced into an isolated freshwater pond. Therefore behavioural isolation can evolve very rapidly among the lateral plate phenotypes of Gasterosteus aculeatus.

A new model of lateral plate morph inheritance in the threespine stickleback,Gasterosteus aculeatus

The threespine stickleback,Gasterosteus aculeatus, is polymorphic for the arrangement of lateral bony plates. It is confirmed in this paper that four morphs (not three) should be distinguished in this species: low plated, low plated with a keel, partially plated and completely plated. A new model is proposed to explain the inheritance of these morphs which involves one major gene with three alleles displaying a dominance hierarchy withA (completely plated) dominant toa (low plated) which is dominant toa k (low plated with keel). The dominance of theA allele is modified to semidominance by a dominant alleleC at a second locus. This scheme explains all the results of relevant breeding experiments published so far. Field data also fulfill predictions derived from this model.

Lateral plate morph differentiation of freshwater and marine populations of the three‐spined stickleback, Gasterosteus aculeatus, in Poland

The distribution of three main lateral plate morphs of the three–spined stickleback, Gasterosteus aculeatus, in the Polish zone of the Baltic Sea and inland waters is surveyed. Most sites are characterized by predominance of the completely plated morph, although it is only in the Vistula River drainage basin where monomorphic complete populations prevail. Polymorphic populations with a high proportion of the non–complete morphs are found in Puck Bay (the Baltic) and in south–west Poland, Possible causes of this pattern are discussed.

Lateral plate morph differentiation of freshwater and marine populations of the three-spined stickleback, Gasterosteus aculeatus, in Poland

The distribution of three main lateral plate morphs of the three–spined stickleback, Gasterosteus aculeatus, in the Polish zone of the Baltic Sea and inland waters is surveyed. Most sites are characterized by predominance of the completely plated morph, although it is only in the Vistula River drainage basin where monomorphic complete populations prevail. Polymorphic populations with a high proportion of the non–complete morphs are found in Puck Bay (the Baltic) and in south–west Poland, Possible causes of this pattern are discussed.

Unusual Lateral Plate Variation of Threespine Sticklebacks (Gasterosteus aculeatus) from Knik Lake, Alaska

Lateral plate phenotypes of Gasterosteus aculeatus from Knik Lake, Alaska form a continuum which cannot be divided objectively to conform to the trimorphic lateral plate morph concept in current use. This case indicates the range of possible lateral plate phenotypes possible in G. aculeatus and brings into question the general applicability of the lateral plate morph concept and underlying genetic models for lateral plate trimorphism. We consider the possibility that abdominal and caudal keel plate phenotypes are potentially genetically independent and that a polygenic model for plate phenotypes may be more appropriate. Pronounced directional asymmetry of lateral plate number was observed in specimens with greater than seven plates per side. This asymmetry does not have obvious functional significance. We suggest that this and other cases of pronounced directional asymmetry may represent stochastic fixation in phylogeny and thus may be useful characters in systematics.

LATERAL PLATE MORPH VARIATION IN CALIFORNIA POPULATIONS OF THE THREESPINE STICKLEBACK, GASTEROSTEUS ACULEATUS.

Marine and anadromous populations of Gasterosteus aculeatus tend to be morphologically uniform, whereas freshwater populations inhabit diverse environments and exhibit great morphological variability (Bell, 1976a, 1984; Wootton, 1976). Although several structures of G. aculeatus vary geographically, the lateral plates have been studied most intensively. They are modified scales that are arranged in a single row along either side of the body. Lateral plate variation includes the lateral plate trimorphism (Hagen and Gilbertson, 1972, 1973), and plate number variation within each of the morphs (Bell, 1984). The complete morph has a continuous row of plates running from the nape onto the caudle peduncle, the partial morph has an abdominal plate row separated from a plate row on the caudal peduncle by an unplated area, and the low morph has only abdominal plates. A genetic basis for lateral plate morph variation has been established (Muinzing, 1959; Hagen and Gilbertson, 1973), and the pattern of geographical variation initially was attributed to divergence in glacial refugia and postglacial secondary intergradation (Miinzing, 1963; Miller and Hubbs, 1969). This explanation has been criticized (Hagen and McPhail, 1970; Bell, 1976a), and Hagen and Moodie ( 1982) suggested an alternative model for the global distribution of lateral plate morphs. They showed that in regions with cold winters and extreme annual temperature ranges, the complete morph dominates and the low morph is virtually absent. In regions with relatively warm winters and consequent low annual temperature flux the low morph is monomorphic. All three morphs occur in intermediate climates. Lateral plate morph frequencies vary markedly over short distances among freshwater populations in regions that harbor all three morphs. Although the functional significance of lateral plate morphs is not understood, the complete morph appears to be associated with more rapidly flowing water than the low morph (Hagen, 1967; Bell, 1982). In this paper we describe spatial variation of lateral plate morphs at two scales. We describe the distribution of the plate morphs among coastal drainages throughout most of the length of California, which includes the transition from low morph monomorphism to trimorphism. Within the cooler northern half of the state, where all three morphs occur, we analyze the distribution of the lateral plate morphs in relation to environmental variation.

Lateral Plate Morph Variation in California Populations of the Threespine Stickleback, Gasterosteus aculeatus

Lateral Plate Morph Variation in California Populations of the Threespine Stickleback, Gasterosteus aculeatus

DIFFERENTIATION OF ADJACENT STREAM POPULATIONS OF THREESPINE STICKLEBACKS.

Corresponding Editor: J. L. Patton

GEOGRAPHIC VARIATION AND ENVIRONMENTAL SELECTION IN GASTEROSTEUS ACULEATUS L. IN THE PACIFIC NORTHWEST, AMERICA.

Ecological geneticists are giving considerable attention to the study of selection in natural populations, its intensity, and what it is capable of doing. Such studies have begun to tell us something about the variation found in natural populations, and how they may adjust to the demands of the prevailing environment. However, these studies have largely been confined to the invertebrates (review in Ford, 1964; Lewontin, 1967; Spiess, 1968; Sheppard, 1969). There is a need for comparative material, and the threespine stickleback (Gasterosteus aculeatus L.) among vertebrates seems to be unusually favorable. Freshwater populations of G. aculeatus are exceedingly variable, and Miller and Hubbs (1969) argued that nearly all the variation is a consequence of introgression between leiurus (freshwater populations) and trackurus (marine populations). But it has become increasingly clear that introgression cannot account for much of the variation in ieiurus (Hagen, 1967; McPhail, 1969; Hagen and McPhail, 1970; Moodie, in press). G. aculeatus is well suited to studies in ecological genetics for its ecology and breeding behavior are easily observed and investigated in the wild. It is unusually abundant, withstands handling and marking very well, and is easily kept and reared in captivity. Its small size facilitates rearing and experimental work in the laboratory, and generation time is relatively short, such that about two generations can be obtained a year. A genetical basis for the more variable traits has been established (Hagen, 1967; McPhail, 1969), and the genetics of several of these (lateral plate number, plate morphs, and gill rakers) is reasonably well known (Hagen, MS; McPhail, unpub. data). Moreover, there is an extensive literature on reproduction, physiology, and life history providing the necessary background (for references see Heuts, 1947; Iersel, 1953; Greenbank and Nelson, 1959; Mullen and Vlugt, 1964; Baggerman, 1966; Assem, 1967). This report is a preliminary investigation of geographic variation in permanent freshwater populations of G. aculeatus, excluding the marine trachurus. The study seeks to establish correlations of phenotype with environmental variables, where they exist, applying the techniques so profitably exploited by ecological geneticists. The importance of introgression as a cause of the variation in leiurus is considered since the data are also relevant to this question.