Body Size and the Maintenance of Reproductive Isolation in Stickleback,Genus Gasterosteus

The blackspotted stickleback Gasterosteus wheatlandi and the widely studied threespine stickleback G. aculeatus are sympatric throughout the former’s range and share many aspects of life history and reproductive behaviour. These two species differ significantly in size, with G. wheatlandi of both sexes measured at approximately 60% of the standard length of their G. aculeatus counterparts. This study concentrated on G. wheatlandi courtship behaviour and investigated its role in the maintenance of reproductive isolation with G. aculeatus. Specifically, the roles that (1) female body size plays in influencing male courtship preferences and (2) male body size and behaviour play in female courtship preferences were investigated through dummy and live conspecific and heterospecific stimulus presentations. Male G. wheatlandi courtship preferences are consistent with previously described patterns for G. aculeatus. Males of both species preferentially approach and court the larger of two simultaneously presented live or dummy females. Thus, the smaller G. wheatlandi males are indiscriminate with respect to assortative mate choice; not only preferring to approach and court more fecund conspecific females but, more significantly, G. aculeatus‐sized females. In contrast, females of both species demonstrate strong assortative courtship preferences. When presented with pairs of flask‐enclosed males, females of both species preferentially orient and court the conspecific male over the heterospecific. Similarly, when presented with a conspecific male and a heterospecific male presented singly, females prefer to enter the nest of the conspecific. Systematic analysis of the interactions between these pairs of fish (one male, one female) demonstrates that the breakdown of courtship in heterospecific courtship occurs late in the courtship sequence when the widely differing forms of male leading behaviour results in drastically differing female responses. I suggest that, as previously described in G. aculeatus, the supernormality effect plays a significant role in mediating adaptive mate choice behaviour in G. wheatlandi. However, the added element of a larger sympatric species introduces a possible cost in time and energy devoted to courting heterospecific, and sympatric, females that the larger G. aculeatus do not likely incur. There is substantial evidence from many sympatric G. aculeatus species pairs that there is assortative mate choice based on size and/or courtship behaviour. Courtship trials suggest a more pervasive role for females in assortative mate choice. Whether it is male body size per se, or in combination with behaviour, morphology or other cues, is unresolved in the present study.     

Distinct spawning migration patterns in sympatric Japan Sea and Pacific Ocean forms of threespine stickleback Gasterosteus aculeatus

Spawning migration patterns were compared between sympatric populations of the anadromous Japan Sea (JS) form and Pacific Ocean (PO) form of the threespine stickleback Gasterosteus aculeatus in the Lake Akkeshi–Bekanbeushi River system, eastern Hokkaido, Japan. In Akkeshi Bay and Lake Akkeshi, the JS form had longer collecting peak periods and more collection peaks than the PO form. Furthermore, although the PO form migrated upstream in freshwater habitats, the greater part of the JS form stayed in brackish waters before breeding. These findings suggest that the 2 forms have distinctly different spawning migration patterns and breeding grounds.     

Neomysis integer in a shallow hypertrophic brackish lake: distribution and predation by three-spined stickleback (Gasterosteus aculeatus)

The mysid shrimp Neomysis integer is a common invertebrate predator in brackish waters of Western Europe and is thought to play a central role in the food web owing to its predation on zooplankton. Neomysis distribution and abundance were investigated for 3 years in brackish, shallow and hypertrophic Lake Ferring (surface area: 3.2 km², mean depth: 1.4 m, salinity: 3–6, total P: 0.29–0.78 mg P l^-1, Secchi depth: 0.14–0.22 m). Mean summer abundance of Neomysis varied from 53 to 882 ind. m^-2. Neomysis density within the lake was relatively uniform and not related to sediment type, but increased with increasing depth. The high abundance of Neomysis is considered to reflect a fish stock almost completely dominated by small-sized fish species (mainly three-spined stickleback, Gasterosteus aculeatus). Three-spined stickleback density was high and catch per unit effort ranged between 30 and 80 per gill net. Stomach analyses showed that the sticklebacks preyed on Neomysis, but preferred specimens smaller than 3–4 mm, and only occasionally consumed those larger than 5–7 mm. In summer, between 33 and 67% of the Neomysis ingested by sticklebacks were smaller than 3 mm, while in the lake as a whole, only 5–14% were smaller than 3 mm. The periods when Neomysis is vulnerable to stickleback predation are restricted to a few weeks in late May and late July, when the new generations emerge. Sticklebacks therefore have a limited capacity for controlling large Neomysis, including gravid females.     

Reproductive tactics of four sympatric sticklebacks (Gasterosteidae)

Synopsis The life history traits (longevity, growth, age at maturity, fecundity, egg size and length of breeding season) were compared for four sympatric sticklebacks (Gasterosteidae). Significant differences occurred for growth, longevity, age at maturity and length of breeding season, but not for egg diameters. Differences in life history traits are interpreted in terms of mechanisms permitting the coexistence of these closely-related territorial fish. Egg numbers were lowest inApeltes quadracus and highest inGasterosteus aculeatus withGasterosteus wheatlandi andPungitius pungitius having similar and intermediate fecundities.     

Implications of a fossil stickleback assemblage for Darwinian gradualism

Darwin postulated that a complete fossil record would contain numerous gradual transitions between ancestral and descendant species, but 150 years after publication of The Origin of Species, few such transitions have materialized. The fossil stickleback Gasterosteus doryssus and the deposit in which it occurs provide excellent conditions to detect such transitions. Abundant, well‐preserved fossils occur in a stratigraphic setting with fine temporal resolution. The paleoecology of G. doryssus resembles the ecology of modern lakes that harbour the phenotypically similar three‐spined stickleback Gasterosteus aculeatus. Gasterosteus aculeatus are primitively highly armoured, but G. doryssus comprised two contemporaneous biological species with relatively weak armour, including a near‐shore, benthic feeder (benthic) and an offshore planktivore (limnetic). The benthic species expanded its range into the limnetic zone of the lake, where it apparently switched to planktivory and evolved reduced armour within c. 5000 years in response to directional selection. Although gradual evolution of mean phenotypes occurred, a single major gene caused much of evolutionary change of the pelvic skeleton. Thus, Darwin's expectation that transitions between species in the fossil record would be gradual was met at a fine time scale, but for pelvic structure, a well‐studied trait, his expectation that gradual change would depend entirely on numerous, small, heritable differences among individuals was incorrect.     

The colonization of two new brackish water habitats on the isle of Texel (the Netherlands)

Summary As a result of the reconstruction of a dike on the Dutch island of Texel two small areas of the Wadden Sea were embanked in 1977 and 1978. In 1981 both by now blocked brackish waters were investigated for macrofauna and macroflora. The vegetation on these former parts of the Wadden Sea was still in a colonizing state. Many small patches ofRuppia spp. were found, contrary to older brackish waters with more extendedRuppia beds. The striking dominance ofR.maritima agrees with its large seed production enabling to colonize quickly new areas. In one of the ponds, where the maximum salinity of 23 Cl^– exceeded far the tolerance limit of this species given in the literature (15 Cl^–),R.maritima was still more numerous thanR.cirrhosa, a species which is more tolerant to salinity fluctuations. Several years after isolation these areas are still inhabited by a few Wadden Sea macrofauna species (e.g. Carcinus maenas, Hydrobia ulvae andCapitella capitata) who managed to survive the drastic environmental changes. In addition, a large number of species characteristic for blocked brackish waters has already colonized the new ponds. One of the two, that has always completely been isolated from other inland water, was inhabited in 1981 by 13 brackish water species. In the future the two new ponds on Texel are expected to loose their pioneer characteristics. There are reasons to expect that most of the Wadden Sea macrofauna relics will soon become extinct. A more extendedRuppia vegetation will probably develop together with a relative increase ofRuppia cirrhosa.     

Sea‐run migratory behaviour in the Japan Sea form of three‐spined stickleback Gasterosteus aculeatus in the tidal pool of eastern Hokkaido Island,Japan

Juveniles in the Japan Sea form of three‐spined stickleback Gasterosteus aculeatus collected from a tidal pool in eastern Hokkaido Island, Japan, had a unimodal standard length (L_S) frequency distribution in each period, ranging from 11·9 to 31·6 mm, and those of sea‐run migrating individuals collected from the outlet of this tidal pool ranged from 17·0 to 36·0 mm, suggesting juveniles of this form would migrate towards the sea when they reached >17·0 mm. In general linear models (GLM) for testing the best model, there was a relationship between the number of sea‐run migratory individual and precipitation, which suggests that precipitation may trigger migration.     

The Response of Prolactin,ACTH, and Growth Hormone Cells in the Pituitary Gland of the Three-Spined Stickleback,: Gasterosteus aculeatus L. form leiurus,to Increased Environmental Salinities

Benjamin, M. 1980. The response of prolactin, ACTH, and growth hormone cells in the pituitary gland of the three-spined stickleback, Gasterosteus aculeatus L. form leiurus, to increased environmental salinities. (Department of Anatomy, University College, Cardiff, Wales, U.K.) — Acta zool. (Stockh.) 61(1): 1–7. The time-sequence of response of the prolactin, ACTH and growth hormone cells in the pituitary gland of the leiurus form of the three-spined stickleback, Gasterosteus aculeatus L., to a transfer from freshwater to seawater, was studied by light microscopy. The appearance of the pituitary was compared with that of animals caught in brackish or sea water. The prolactin cells respond only slowly to seawater by cytological changes interpreted as signs of decreased secretory activity. It is thus suggested that prolactin is unlikely to be important for osmoregulation in this stickleback. The growth hormone cells are more active in all seawater-adapted animals, while the ACTH cells are less active—although only in laboratory experiments. The differing responses of the pituitaries of the leiurus and trachurus forms of G. aculeatus and Pungitius pungitius to high salinities are compared. Even in species whose pituitaries are virtually identical, the response to high salinites may differ widely.     

Total evidence phylogeny of Gasterosteidae: combining molecular, morphological and behavioral data

Genealogical relationships among Gasterosteidae (Teleostei: Gasterosteiformes) were tested with 84 morphological, 48 behavioral, and 2879 molecular characters. Phylogenetic analysis of the combined data set identified a single (CI = 0.735) best‐supported hypothesis (Spinachia (Apeltes ((Pungitius + Culaea)(Gasterosteus aculeatus + G. wheatlandi)))). This hypothesis is identical to previous phylogenetic propositions proposed on the basis of behavioral, and behavioral plus morphological data. Our hypothesis, however, differed from a molecular‐based phylogeny in the placement of Apeltes. This analysis highlights the importance of combining all available evidence in order to produce the best‐supported proposition of genealogical relationships.     

A part of the Japan Sea form of the threespine stickleback, Gasterosteus aculeatus, spawns in the seawater tidal pools of western Hokkaido Island, Japan

The Japan sea form of the threespine stickleback, Gasterosteus aculeatus, was found to spawn in the seawater tidal pool of the Cape Benkei, western Hokkaido Island, Japan, in 2001 and 2003. Nest-guarding males, adult females and juveniles of this form were also observed in four tidal pools of the Capes Benkei, Kabuto and Kamui, in 2001–2003. Otolith Sr:Ca ratios in sticklebacks collected from these tidal pools were relative high from the core to the edge, suggesting they lived in seawater environments throughout its life cycle. These findings suggest that a part of the Japan Sea formȁ9s individuals in western Hokkaido Island have the potential to breed in the coastal sea and the life history style has evolved in dependence on the seawater environment.     

Growth history and migration of the threespine stickleback <Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis> in Otsuchi Bay,northeastern Japan

 Both growth and migratory history of the Pacific Ocean forms of the threespine stickleback Gasterosteus aculeatus collected in Otsuchi Bay, northeastern Japan, were examined using otolith microstructure and analysis of strontium (Sr) and calcium (Ca) concentrations with wavelength dispersive X-ray spectrometry by an electron microprobe. Age of the juveniles (21.6–25.9 mm in total length) examined ranged from 101 to 128 days (115 ± 8.5 days; mean ± SD), hatching being estimated as having occurred between March and April 2001. The Sr : Ca ratios in the otoliths changed with both ontogenic development and salinity of the habitat. The otolith Sr : Ca ratios increased gradually from 4.1 × 10⁻³ around the core to 7.5 × 10⁻³ around the edge of the otolith. The fluctuation pattern of otolith Sr : Ca ratios was different from those observed in both freshwater resident and anadromous forms in previous studies. These results suggested that the fish sampled spend their lives in the estuarine and sea environment without freshwater life after hatching. Received: June 5, 2002 / Revised: September 11, 2002 / Accepted: September 24, 2002 Acknowledgments We thank Mr. K. Morita and crews of the Otsuchi Marine Research Center, Ocean Research Institute, The University of Tokyo for their assistance in collecting specimens. This work was supported in part by Grant-in-Aid No. 13760138 from the Ministry of Education, Culture, Sports, Science and Technology, Japan. Correspondence to:Takaomi Arai     

Biology of four sympatric sticklebacks in Cobscook Bay,Maine, a boreal,macrotidal bay

Four species of sticklebacks were collected during May, June, August, and September 2011–2013 in a survey of fishes of Cobscook Bay, a macrotidal bay in eastern Maine, U.S.A. Threespine (Gasterosteus aculeatus) and ninespine (Pungitius pungitius) sticklebacks have circumpolar distributions; blackspotted (Gasterosteus wheatlandi) and fourspine (Apeltes quadracus) sticklebacks are limited to northeastern North America. Sticklebacks were collected in the intertidal zone with beach seines and in the pelagic zone with trawls. Up to 30 individuals of each species from each sample were measured and weighed. Individuals were identified as gravid or not in 2012 and 2013. Catch-per-unit-efforts of the most abundant threespine (18,878 individuals) and second most abundant blackspotted sticklebacks (2433) were greatest in the innermost part of the bay, on mudflats, in 2012, and in August. Fewer than 100 fourspine and fewer than 50 ninespine sticklebacks were caught over the three years, mostly in the inner bay. Length-frequency distributions suggested age classes of 0+, 1+, 2+ and a few 3+ for threespine sticklebacks and 0+ and 1+ for blackspotted sticklebacks. Most gravid individuals of those two species were present in May and June. Spawning occurred earlier in 2012, an unusually warm year, than in 2013. Changes in presence, timing, and abundance of other species in the fish survey corroborated the influence of the record warm conditions in 2012 in the Gulf of Maine on the fish community of Cobscook Bay. Blackspotted and ninespine sticklebacks are vulnerable to population decline from warming in the Gulf of Maine because they are near the southern limits of distribution.     

Migratory history of the threespine stickleback Gasterosteus aculeatus

 The migratory history of two highly divergent forms (the Japan Sea and Pacific Ocean forms) of the threespine stickleback Gasterosteus aculeatus collected from Japanese brackish water (seawater) and freshwater was studied by examining strontium (Sr) and calcium (Ca) concentrations in their otoliths using wavelength dispersive X-ray spectrometry on an electron microprobe. The Sr : Ca ratios in the otoliths changed with salinity of the habitat. The otolith Sr : Ca ratios of the freshwater resident-type samples of the Pacific Ocean form showed consistently low Sr : Ca ratios, averaging 0.85–0.96 × 10⁻³ from the core to the edge. In contrast, the otolith Sr : Ca ratios of the anadromous type of both the Japan Sea and Pacific Ocean forms fluctuated strongly along the life history transects in accordance with their migration patterns from seawater to freshwater. The higher ratios in the anadromous type, averaging 5.4 × 10⁻³, in the otolith region from the core to 200 μm, corresponded to the seagoing period, suggesting that otolith Sr : Ca ratios are affected by ambient water salinity. These findings clearly indicate that otolith Sr : Ca ratios reflect individual life histories, and that these two highly divergent forms of stickleback have a flexible migration strategy. Received: May 23, 2002 / Revised: July 29, 2002 / Accepted: August 19, 2002 Acknowledgments We are grateful to Dr. S. Mori of Gifu Keizai University, and Miss M. Yamada and Messrs. M. Kume and T. Kitamura of Hokkaido University, for their assistance in sampling. This work was supported in part by Grant-in-Aid No. 13760138 from the Ministry of Education, Culture, Sports, Science and Technology, Japan. Correspondence to:Takaomi Arai     

Speciation in ninespine stickleback: reproductive isolation and phenotypic divergence among cryptic species of Japanese ninespine stickleback

Although similar patterns of phenotypic diversification are often observed in phylogenetically independent lineages, differences in the magnitude and direction of phenotypic divergence have been also observed among independent lineages, even when exposed to the same ecological gradients. The stickleback family is a good model with which to explore the ecological and genetic basis of parallel and nonparallel patterns of phenotypic evolution, because there are a variety of populations and species that are locally adapted to divergent environments. Although the patterns of phenotypic divergence as well as the genetic and ecological mechanisms have been well characterized in threespine sticklebacks, Gasterosteus aculeatus, we know little about the patterns of phenotypic diversification in other stickleback lineages. In eastern Hokkaido, Japan, there are three species of ninespine sticklebacks, Pungitius tymensis and the freshwater type and the brackish‐water type of the P. pungitius–P. sinensis species complex. They utilize divergent habitats along coast–stream gradients of rivers. Here, we investigated genetic, ecological and phenotypic divergence among three species of Japanese ninespine sticklebacks. Divergence in trophic morphology and salinity tolerance occurred in the direction predicted by the patterns observed in threespine sticklebacks. However, the patterns of divergence in armour plate were different from those previously found in threespine sticklebacks. Furthermore, the genetic basis of plate variation may differ from that in threespine sticklebacks. Because threespine sticklebacks are well‐established model for evolutionary research, the sympatric trio of ninespine sticklebacks will be an invaluable resource for ecological and genetic studies on both common and lineage‐specific patterns of phenotypic diversification.     

Morphological characteristics of an introduced threespine stickleback,Gasterosteus aculeatus,from Hasse Lake,Alberta: a first occurrence in the interior plains of North America

Synopsis Threespine stickleback, Gasterosteus aculeatus, are thought to have been introduced into Hasse Lake, Alberta, where they were discovered in 1980. The population has grown in numbers since 1980 and by 1981 was more abundant than the native brook stickleback, Culaea inconstans. This population is the first to be found in the interior plains of North America, and it occurs at a higher elevation than any other Canadian population. The source of this introduced population is unknown. Significant differences among four years were found in several meristic and morphometric characters but no significant trends during 1980–1983 were found. Most characters were well within the range of other populations of the species.     

Genetic and morphometric divergence in threespine stickleback in the Chignik catchment,Alaska

Divergent selection pressures induced by different environmental conditions typically lead to variation in life history, behavior, and morphology. When populations are locally adapted to their current environment, selection may limit movement into novel sites, leading to neutral and adaptive genetic divergence in allopatric populations. Subsequently, divergence can be reinforced by development of pre‐ or postzygotic barriers to gene flow. The threespine stickleback, Gasterosteus aculeatus, is a primarily marine fish that has invaded freshwater repeatedly in postglacial times. After invasion, the established freshwater populations typically show rapid diversification of several traits as they become reproductively isolated from their ancestral marine population. In this study, we examine the genetic and morphometric differentiation between sticklebacks living in an open system comprising a brackish water lagoon, two freshwater lakes, and connecting rivers. By applying a set of microsatellite markers, we disentangled the genetic relationship of the individuals across the diverse environments and identified two genetic populations: one associated with brackish and the other with the freshwater environments. The “brackish” sticklebacks were larger and had a different body shape than those in freshwater. However, we found evidence for upstream migration from the brackish lagoon into the freshwater environments, as fish that were genetically and morphometrically similar to the lagoon fish were found in all freshwater sampling sites. Regardless, few F1‐hybrids were identified, and it therefore appears that some pre‐ and/or postzygotic barriers to gene flow rather than geographic distance are causing the divergence in this system.     

Egg-brooding, body size and predation risk in planktonic marine copepods

We investigated the interacting effects of copepod body size and the presence or absence of egg masses on the risk of predation by a visual predator. We conducted selection experiments involving three-spined sticklebacks (Gasterosteus aculeatus) and copepods ranging in body mass from 0.5 to 740 μg C: Oithona similis, Corycaeus anglicus, Pseudocalanus newmani, P. moultoni, Pseudodiaptomus marinus, and Paraeuchaeta elongata. We found that sticklebacks selected ovigerous females of the two smallest-bodied species of copepods (Oithona similis and Corycaeus anglicus). In contrast, the fish showed no significant selection for ovigerous females of the remaining, larger-bodied species. Unexpectedly, egg mass position (i.e., in a ventral, dorsal or lateral location on the urosome) appeared to influence predation risk more than did body size, resulting in higher predation risk for the cyclopoid and poecilostomatoid species than for the calanoid species we tested. Although the sticklebacks showed no statistically significant preference for ovigerous females of any of the four calanoid species, for each species the overall proportion of ovigerous females ingested was slightly greater than 0.50. Thus, whether body size influences the susceptibility of egg-brooding calanoid copepods to predation remains an open question. Received: 24 August 1998 / Accepted: 6 July 1999     

Parasites and parallel divergence of the number of individual MHC alleles between sympatric three‐spined stickleback Gasterosteus aculeatus morphs in Iceland

Two pairs of sympatric three‐spined stickleback Gasterosteus aculeatus morphs and two single morph populations inhabiting mud and lava or rocky benthic habitats in four Icelandic lakes were screened for parasites and genotyped for MHC class IIB diversity. Parasitic infection differed consistently between G. aculeatus from different benthic habitats. Gasterosteus aculeatus from the lava or rocky habitats were more heavily infected in all lakes. A parallel pattern was also found in individual MHC allelic variation with lava G. aculeatus morphs exhibiting lower levels of variation than the mud morphs. Evidence for selective divergence in MHC allele number is ambiguous but supported by two findings in addition to the parallel pattern observed. MHC allele diversity was not consistent with diversity reported at neutral markers (microsatellites) and in Þingvallavatn the most common number of alleles in each morph was associated with lower infection levels. In the Þingvallavatn lava morph, lower infection levels by the two most common parasites, Schistocephalus solidus and Diplostomum baeri, were associated with different MHC allele numbers.     

Exploring Jordan's rule in Pacific three‐spined stickleback Gasterosteus aculeatus

Coastal marine Gasterosteus aculeatus were captured from seven locations along the Pacific coast of North America, ranging across 21·8° latitude to test Jordan's rule, i.e. that vertebral number should increase with increasing latitude for related populations of fish. Vertebral number significantly increased with increasing latitude for both total and caudal vertebral number. Increasing length with latitude (sensu Bergmann's rule) was also supported, but the predictions for Jordan's rule held when controlling for standard length. Pleomerism was weakly evidenced. Gasterosteus aculeatus exhibited sexual dimorphism for Jordan's rule, with both sexes having more vertebrae at higher latitudes, but only males showing a positive association between latitude and the ratio of caudal to abdominal vertebrae. The number of dorsal‐ and anal‐fin rays and basals increased with increasing latitude, while pectoral‐fin ray number decreased. This study reinforces the association between phenotypic variation and environmental variation in marine populations of G. aculeatus.     

Extensive lineage-specific gene duplication and evolution of the spiggin multi-gene family in stickleback

Background  

The threespine stickleback (Gasterosteus aculeatus) has a characteristic reproductive mode; mature males build nests using a secreted glue-like protein called spiggin. Although recent studies reported multiple occurrences of genes that encode this glue-like protein spiggin in threespine and ninespine sticklebacks, it is still unclear how many genes compose the spiggin multi-gene family.