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Life history, ecology and the biogeography of strong genetic breaks among 15 species of Pacific rockfish, Sebastes

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Abstract

Strong genetic change over short spatial scales is surprising among marine species with high dispersal potential. Concordant breaks among several species signals a role for geographic barriers to dispersal. Along the coast of California, such breaks have not been seen across the biogeographic barrier of Point Conception, but other potential geographic boundaries have been surveyed less often. We tested for strong-population structure in 11 species of Sebastes sampled across two regions containing potential dispersal barriers, and conducted a meta-analysis including four additional species. We show two strong breaks north of Monterey Bay, spanning an oceanographic gradient and an upwelling jet. Moderate genetic structure is just as common in the north as it is in the south, across the biogeographic break at Point Conception. Gene flow is generally higher among deep-water species, but these conclusions are confounded by phylogeny. Species in the subgenus Sebastosomus have higher structure than those in the subgenus Pteropodus, despite having larvae with longer pelagic phases. Differences in settlement behavior in the face of ocean currents might help explain these differences. Across similar species across the same coastal environment, we document a wide variety of patterns in gene flow, suggesting that interaction of individual species traits such as settlement behavior with environmental factors such as oceanography can strongly impact population structure.

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Acknowledgments

We wish to thank the crews of Stardust Sportfishing (Santa Barbara, CA), Chris’ Fishing Trips (Monterey, CA) and Garibaldi Charters (Garibaldi, OR) for assistance in sample collection. We also thank D. Pearse, R. Vetter, M. O. Burford and M. Johansson for providing additional samples. Members of the Palumbi lab provided useful feedback and discussion. We thank M. McManus, M. Carr and P. Raimondi for sharing unpublished data. This study was funded by a grant to SRP from the Andrew W. Mellon Foundation and by the Partnership for Interdisciplinary Studies of Coastal Oceans (PISCO) under grants from the David and Lucille Packard Foundation, and the Gordon and Betty Moore Foundation.

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  1. Department of Biological Sciences, Hopkins Marine Station, Stanford University, 120 Oceanview Boulevard, Pacific Grove, CA, 93950, USA

    Arjun Sivasundar & Stephen R. Palumbi

  2. Division of Aquatic Ecology, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012, Bern, Switzerland

    Arjun Sivasundar

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  1. Arjun Sivasundar
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Correspondence to Arjun Sivasundar.

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Communicated by M. I. Taylor.

Appendix: Results for individual species

Appendix: Results for individual species

(1) Population structure in shallow-water species

Blue rockfish S. mystinus

The large estimates for Φ ST between OR and MB populations of blue rockfish (0.2468; P < 0.05) and between OR and SB populations (0.1862; P < 0.05), but not between MB and SB (0.0235; not significant) reflect the clustering evident in the phylogenetic tree. In concordance with the results from control region data, microsatellite data revealed strong genetic differentiation between OR and the other populations of blue rockfish at every individual locus. Assignment tests further corroborated these patterns. Differentiation between OR and MB was extremely strong and highly significant (P < 0.0001), and present but less marked between SB and MB (P < 0.003).

Black rockfish S. melanops

For black rockfish, there was a small but significant genetic differentiation between MB and OR (Φ ST = 0.045; P < 0.05). A single microsatellite locus, Sra7-7, showed significant differentiation between MB and OR populations of black rockfish (F ST = 0.029; P < 0.05). None of the other loci revealed significant differentiation between the populations, and nor did joint analysis of all loci. Assignment tests corroborated these patterns, with genotype assignment not significantly different from random (P = 0.141).

Olive rockfish S. serranoides

For olive rockfish samples from MB and SB, there was little evidence of mtDNA differentiation (Φ ST = 0.010; not significant). As with black rockfish, the microsatellite locus, Sra7-7, also showed a statistically significant estimate of genetic differentiation between MB and SB populations. When all loci were jointly analyzed for this species, however, there was weak, but statistically significant differentiation (F ST = 0.010; P < 0.05) between populations. Assignment of genotypes to populations in this species was significantly non-random (P = 0.004).

Copper rockfish S. caurinus

The OR and MB populations were both genetically differentiated from the SB populations for mtDNA (Φ ST = 0.072 and 0.121, respectively, P < 0.05), but the MB and OR populations could not be distinguished from each other (Φ ST = 0.021). Microsatellite data from copper rockfish from three locations did not reveal the genetic differentiation: one locus was significantly different between OR and SB (Sma10; F ST = 0.065; P < 0.05), but joint analyses did not support this, or any other pairwise differentiation. The assignment tests, however, showed a slight differentiation between OR and MB populations, but not between MB and SB. Though our sample sizes are low for this species, similarly low genetic differentiation was reported by Buonaccorsi et al. (2002), who found only slight differentiation among populations from northern to southern California (F ST = 0.009, P < 0.003).

Gopher rockfish S. carnatus

There was evidence for mild genetic differentiation in Gopher rockfish mtDNA (Φ ST = 0.064; P < 0.05). However, joint analysis of all microsatellite loci did not reveal any significant differentiation between these populations nor did genotype assignments differ significantly from random expectations (P = 0.083).

Brown rockfish S. auriculatus

In the third species in this subgroup, there was no significant mtDNA differentiation. Populations of brown rockfish from MB and SB were significantly differentiated at the microsatellite locus Sma5 (F ST = 0.092; P < 0.05), but not at any of the other loci. When the five loci were combined, however, there was a significant genetic difference between populations (F ST = 0.022; P < 0.05). There was also a highly significant difference between populations as assessed by the assignment test (P < 0.0001).

(2) Population structure in deep-water species

Only the yellowtail rockfish showed structure in our survey of five deep-water species, and this structure was very high. However, vermillion rockfish showed a striking pattern of deviation from Hardy–Weinberg equilibrium, and the presence of strikingly different mtDNA clade in Santa Barbara that suggests multiple gene pools in these collections.

Yellowtail rockfish S. flavidus

The differentiation of mtDNA of yellowtail rockfish from OR and the other populations is borne out by the large estimates for Φ ST between OR and MB (0.2542; P < 0.05) and between OR and SB (0.1909; P < 0.05), but not between MB and SB (−0.0141, not significant). As with control region data, microsatellite data from yellowtail rockfish again revealed strong evidence of genetic differentiation between MB and OR samples. There was significant differentiation between these two populations at three of the loci considered individually (Sal2, Sra7-2 and Sma4), and when all loci were considered jointly, excluding one locus that was not in HWE, there was high and significant differentiation whether measured as R ST (0.028; P < 0.05) or F ST (0.094; P < 0.05). The same three loci also showed some differentiation between SB and OR, but joint analysis of all loci did not yield any significant differentiation between these populations. Between MB and SB, a single locus (Sal2) had a significant R ST value. Results from the assignment tests revealed the same patterns. Differentiation between OR and MB was marked and highly significant (P < 0.0001), while MB and SB were not significantly differentiated (P = 0.061).

Widow rockfish S. entomelas

The widow rockfish showed no patterns of genetic differentiation. There was no evidence for mtDNA differentiation between the populations (Φ ST = −0.024). Microsatellite loci also failed to reveal any differentiation among populations either. A single locus, Sma10, differed slightly between populations (F ST = 0.087; P < 0.05). Joint analysis of all loci failed to reveal differentiation between the populations, whether examined by F ST and R ST or by assignment tests (P = 0.197).

Bocaccio S. paucispinis

Bocaccio had lower haplotype diversity than most other species, and there was no evidence for mtDNA differentiation between MB and SB (Φ ST = −0.019). With microsatellites, bocaccio from MB and SB showed only slight differences between populations. While joint analysis of microsatellite loci failed to reveal genetic differentiation using F-statistics, a single locus differed between populations (F ST = 0.081; R ST = 0.109; P < 0.05). Genotype assignment tests, however, were significantly non-random in assigning individuals to their populations of origin (P = 0.011). Matala et al. (2004) used microsatellites to show low but significant differentiation of bocaccio along the California coast…

Starry rockfish S. constellatus

Starry rockfish exhibited high haplotype diversity (H = 0.986) with only two haplotypes shared between the populations, as opposed to 17 (in MB) and 20 (SB) private haplotypes. One of the MB haplotypes, which occurs twice in those samples, was highly divergent from all others. There was also no evidence of genetic differentiation between the populations (Φ ST = 0.000). Starry rockfish was the only species which failed to reveal any evidence of population substructuring, whether microsatellite loci were considered individually or jointly. The same was true of the assignment tests, where genotype assignments occurred exactly as expected by chance (P = 1.000).

Vermilion rockfish S. miniatus

A number of unusual patterns emerged for vermilion rockfish (Table 5).

Table 5 Pairwise measures of population differentiation in Sebastes spp
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Sivasundar, A., Palumbi, S.R. Life history, ecology and the biogeography of strong genetic breaks among 15 species of Pacific rockfish, Sebastes . Mar Biol 157, 1433–1452 (2010). https://doi.org/10.1007/s00227-010-1419-3

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