scholarly journals Oceans apart: Heterogeneous patterns of parallel evolution in sticklebacks

2019 ◽  
Author(s):  
Bohao Fang ◽  
Petri Kemppainen ◽  
Paolo Momigliano ◽  
Xueyun Feng ◽  
Juha Merilä

AbstractAn important model system for the study of genomic mechanisms underlying parallel ecological adaptation in the wild is the three-spined stickleback (Gasterosteus aculeatus), which has repeatedly colonized and adapted to freshwater from the sea throughout the northern hemisphere. Previous studies have identified numerous genomic regions showing consistent genetic differentiation between freshwater and marine ecotypes, but these are typically based on limited geographic sampling and are biased towards studies in the Eastern Pacific. We analysed population genomic data from marine and freshwater ecotypes of three-spined sticklebacks with from a comprehensive global collection of marine and freshwater ecotypes to detect loci involved in parallel evolution at different geographic scales. Our findings highlight that most signatures of parallel evolution were unique to the Eastern Pacific. Trans-oceanic marine and freshwater differentiation was only found in a very limited number of genomic regions, including three chromosomal inversions. Using both simulations and empirical data, we demonstrate that this is likely due to both the stochastic loss of freshwater-adapted alleles during founder events during the invasion of the Atlantic basin and selection against freshwater-adapted variants in the sea, both of which have reduced the amount of standing genetic variation available for freshwater adaptation outside the Eastern Pacific region. Moreover, the existence of highly elevated linkage disequilibrium associated with marine-freshwater differentiation in the Eastern Pacific is also consistent with a secondary contact scenario between marine and freshwater populations that have evolved in isolation from each other during past glacial periods. Thus, contrary to what earlier studies focused on Eastern Pacific populations have led us to believe, parallel marine-freshwater differentiation in sticklebacks is far less prevalent and pronounced in all other parts of the species global distribution range.

Genetics ◽  
1998 ◽  
Vol 150 (2) ◽  
pp. 807-814
Author(s):  
Adalgisa Caccone ◽  
Gi-Sik Min ◽  
Jeffrey R Powell

Abstract For more than 60 years, evolutionary cytogeneticists have been using naturally occurring chromosomal inversions to infer phylogenetic histories, especially in insects with polytene chromosomes. The validity of this method is predicated on the assumption that inversions arise only once in the history of a lineage, so that sharing a particular inversion implies shared common ancestry. This assumption of monophyly has been generally validated by independent data. We present the first clear evidence that naturally occurring inversions, identical at the level of light microscopic examination of polytene chromosomes, may not always be monophyletic. The evidence comes from DNA sequence analyses of regions within or very near the breakpoints of an inversion called the 2La that is found in the Anopheles gambiae complex. Two species, A. merus and A. arabiensis, which are fixed for the “same” inversion, do not cluster with each other in a phylogenetic analysis of the DNA sequences within the 2La. Rather, A. merus 2La is most closely related to strains of A. gambiae homozygous for the 2L+. A. gambiae and A. merus are sister taxa, the immediate ancestor was evidently homozygous 2L+, and A. merus became fixed for an inversion cytologically identical to that in A. arabiensis. A. gambiae is polymorphic for 2La/2L+, and the 2La in this species is nearly identical at the DNA level to that in A. arabiensis, consistent with the growing evidence that introgression has or is occurring between these two most important vectors of malaria in the world. The parallel evolution of the “same” inversion may be promoted by the presence of selectively important genes within the breakpoints.


2014 ◽  
Vol 281 (1783) ◽  
pp. 20140012 ◽  
Author(s):  
Devon E. Pearse ◽  
Michael R. Miller ◽  
Alicia Abadía-Cardoso ◽  
John Carlos Garza

Rapid adaptation to novel environments may drive changes in genomic regions through natural selection. Such changes may be population-specific or, alternatively, may involve parallel evolution of the same genomic region in multiple populations, if that region contains genes or co-adapted gene complexes affecting the selected trait(s). Both quantitative and population genetic approaches have identified associations between specific genomic regions and the anadromous (steelhead) and resident (rainbow trout) life-history strategies of Oncorhynchus mykiss . Here, we use genotype data from 95 single nucleotide polymorphisms and show that the distribution of variation in a large region of one chromosome, Omy5, is strongly associated with life-history differentiation in multiple above-barrier populations of rainbow trout and their anadromous steelhead ancestors. The associated loci are in strong linkage disequilibrium, suggesting the presence of a chromosomal inversion or other rearrangement limiting recombination. These results provide the first evidence of a common genomic basis for life-history variation in O. mykiss in a geographically diverse set of populations and extend our knowledge of the heritable basis of rapid adaptation of complex traits in novel habitats.


1993 ◽  
Vol 71 (3) ◽  
pp. 515-523 ◽  
Author(s):  
J. D. McPhail

Pairs of plankton-feeding and benthos-foraging sticklebacks (Gasterosteus aculeatus) (limnetics and benthics) coexist in six small lakes in southwestern British Columbia. In spite of a persistent low level of hybridization the pairs maintain themselves as distinct genetic and ecological entities; because of this they are viewed as biological species. They appear to be restricted to the central Strait of Georgia region, and the geological history of the area argues that they are of postglacial origin. The pairs occur on three islands (Vancouver, Texada, and Lasqueti), but even on these islands they are not found in all available lakes. Both lake morphometry (size and depth) and altitude appear to influence local distribution. Hypotheses that might explain the origin of the pairs are examined. Neither theory nor data support a sympatric origin, but an allopatric origin through two invasions of marine sticklebacks is consistent with both the geological history of the area and the details of local distribution. An independent but parallel evolution of the pairs on at least two islands (Vancouver and Texada) is implicit in this hypothesis. The hypothesis also assumes that although the initial divergence started in allopatry, competitive interactions in sympatry played a major role in the evolution of reproductive isolation and resource partitioning.


2019 ◽  
Author(s):  
Antoine Paccard ◽  
Dieta Hanson ◽  
Yoel E. Stuart ◽  
Frank A. von Hippel ◽  
Martin Kalbe ◽  
...  

ABSTRACTThe repeatability of adaptive radiation is expected to be scale dependent, with determinism decreasing as greater spatial separation among “replicates” leads to their increased genetic and ecological independence. Threespine stickleback (Gasterosteus aculeatus) provide an opportunity to test whether this expectation holds for the early stages of adaptive radiation - their diversification in freshwater ecosystems has been replicated many times. To better understand the repeatability of that adaptive radiation, we examined the influence of geographic scale on levels of parallel evolution by quantifying phenotypic and genetic divergence between lake and stream stickleback pairs sampled at regional (Vancouver Island) and global (North America and Europe) scales. We measured phenotypes known to show lake-stream divergence and used reduced representation genome-wide sequencing to estimate genetic divergence. We assessed the scale-dependence of parallel evolution by comparing effect sizes from multivariate models and also the direction and magnitude of lake-stream divergence vectors. At the phenotypic level, parallelism was greater at the regional than the global scale. At the genetic level, putative selected loci showed greater lake-stream parallelism at the regional than the global scale. Generally, the level of parallel evolution was low at both scales, except for some key univariate traits. Divergence vectors were often orthogonal, highlighting possible ecological and genetic constraints on parallel evolution at both scales. Overall, our results confirm that the repeatability of adaptive radiation decreases at increasing spatial scales. We suggest that greater environmental heterogeneity at larger scales imposes different selection regimes, thus generating lower repeatability of adaptive radiation at larger spatial scales.


2019 ◽  
Vol 110 (6) ◽  
pp. 684-695 ◽  
Author(s):  
Alan Garcia-Elfring ◽  
Rowan D H Barrett ◽  
Virginie Millien

Abstract Identifying genetic variation involved in thermal adaptation is likely to yield insights into how species adapt to different climates. Physiological and behavioral responses associated with overwintering (e.g., torpor) are thought to serve important functions in climate adaptation. In this study, we use 2 isolated Peromyscus leucopus lineages on the northern margin of the species range to identify single nucleotide polymorphisms (SNPs) showing a strong environmental association and test for evidence of parallel evolution. We found signatures of clinal selection in each lineage, but evidence of parallelism was limited, with only 2 SNPs showing parallel allele frequencies across transects. These parallel SNPs map to a gene involved in protection against iron-dependent oxidative stress (Fxn) and to a gene with unknown function but containing a forkhead-associated domain (Fhad1). Furthermore, within transects, we find significant clinal patterns in genes enriched for functions associated with glycogen homeostasis, synaptic function, intracellular Ca2+ balance, H3 histone modification, as well as the G2/M transition of cell division. Our results are consistent with recent literature on the cellular and molecular basis of climate adaptation in small mammals and provide candidate genomic regions for further study.


2020 ◽  
Author(s):  
Ryo Kakioka ◽  
Seiichi Mori ◽  
Tomoyuki Kokita ◽  
Takuya K Hosoki ◽  
Atsushi J Nagano ◽  
...  

Abstract Background: The three-spined stickleback (Gasterosteus aculeatus) is a remarkable system to study the genetic mechanisms underlying parallel evolution during the transition from marine to freshwater habitats. Although the majority of previous studies on the parallel evolution of sticklebacks have mainly focused on postglacial freshwater populations in the Pacific Northwest of North America and northern Europe, we recently use Japanese stickleback populations for investigating shared and unique features of adaptation and speciation between geographically distant populations. However, we currently lack a comprehensive phylogeny of the Japanese three-spined sticklebacks, despite the fact that a good phylogeny is essential for any evolutionary and ecological studies. Here, we conducted a phylogenomic analysis of the three-spined stickleback in the Japanese Archipelago.Results: We found that freshwater colonization occurred in multiple waves, each of which may reflect different interglacial isolations. Some of the oldest freshwater populations from the central regions of the mainland of Japan (Hariyo populations) were estimated to colonize freshwater approximately 170,000 years ago. The next wave of colonization likely occurred approximately 100,000 years ago. The inferred origins of several human-introduced populations showed that introduction occurred mainly from nearby habitats. We also found a new habitat of the three-spined stickleback sympatric with the Japan Sea stickleback (Gasterosteus nipponicus).Conclusions: These Japanese stickleback systems differ from those in the Pacific Northwest of North America and northern Europe in terms of divergence time and history. Stickleback populations in the Japanese Archipelago offer valuable opportunities to study diverse evolutionary processes in historical and contemporary timescales.


Science ◽  
2019 ◽  
Vol 363 (6422) ◽  
pp. 81-84 ◽  
Author(s):  
Kathleen T. Xie ◽  
Guliang Wang ◽  
Abbey C. Thompson ◽  
Julia I. Wucherpfennig ◽  
Thomas E. Reimchen ◽  
...  

Evolution generates a remarkable breadth of living forms, but many traits evolve repeatedly, by mechanisms that are still poorly understood. A classic example of repeated evolution is the loss of pelvic hindfins in stickleback fish (Gasterosteus aculeatus). Repeated pelvic loss maps to recurrent deletions of a pelvic enhancer of the Pitx1 gene. Here, we identify molecular features contributing to these recurrent deletions. Pitx1 enhancer sequences form alternative DNA structures in vitro and increase double-strand breaks and deletions in vivo. Enhancer mutability depends on DNA replication direction and is caused by TG-dinucleotide repeats. Modeling shows that elevated mutation rates can influence evolution under demographic conditions relevant for sticklebacks and humans. DNA fragility may thus help explain why the same loci are often used repeatedly during parallel adaptive evolution.


2020 ◽  
Vol 20 (1) ◽  
Author(s):  
Ryo Kakioka ◽  
Seiichi Mori ◽  
Tomoyuki Kokita ◽  
Takuya K. Hosoki ◽  
Atsushi J. Nagano ◽  
...  

Abstract Background The three-spined stickleback (Gasterosteus aculeatus) is a remarkable system to study the genetic mechanisms underlying parallel evolution during the transition from marine to freshwater habitats. Although the majority of previous studies on the parallel evolution of sticklebacks have mainly focused on postglacial freshwater populations in the Pacific Northwest of North America and northern Europe, we recently use Japanese stickleback populations for investigating shared and unique features of adaptation and speciation between geographically distant populations. However, we currently lack a comprehensive phylogeny of the Japanese three-spined sticklebacks, despite the fact that a good phylogeny is essential for any evolutionary and ecological studies. Here, we conducted a phylogenomic analysis of the three-spined stickleback in the Japanese Archipelago. Results We found that freshwater colonization occurred in multiple waves, each of which may reflect different interglacial isolations. Some of the oldest freshwater populations from the central regions of the mainland of Japan (hariyo populations) were estimated to colonize freshwater approximately 170,000 years ago. The next wave of colonization likely occurred approximately 100,000 years ago. The inferred origins of several human-introduced populations showed that introduction occurred mainly from nearby habitats. We also found a new habitat of the three-spined stickleback sympatric with the Japan Sea stickleback (Gasterosteus nipponicus). Conclusions These Japanese stickleback systems differ from those in the Pacific Northwest of North America and northern Europe in terms of divergence time and history. Stickleback populations in the Japanese Archipelago offer valuable opportunities to study diverse evolutionary processes in historical and contemporary timescales.


EvoDevo ◽  
2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Eva Terzibasi Tozzini ◽  
Alessandro Cellerino

AbstractAnnual fishes of the genus Nothobranchius inhabit ephemeral habitats in Eastern and Southeastern Africa. Their life cycle is characterized by very rapid maturation, a posthatch lifespan of a few weeks to months and embryonic diapause to survive the dry season. The species N. furzeri holds the record of the fastest-maturing vertebrate and of the vertebrate with the shortest captive lifespan and is emerging as model organism in biomedical research, evolutionary biology, and developmental biology. Extensive characterization of age-related phenotypes in the laboratory and of ecology, distribution, and demography in the wild are available. Species/populations from habitats differing in precipitation intensity show parallel evolution of lifespan and age-related traits that conform to the classical theories on aging. Genome sequencing and the establishment of CRISPR/Cas9 techniques made this species particularly attractive to investigate the effects genetic and non-genetic intervention on lifespan and aging-related phenotypes. At the same time, annual fishes are a very interesting subject for comparative approaches, including genomics, transcriptomics, and proteomics. The N. furzeri community is highly diverse and rapidly expanding and organizes a biannual meeting.


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