The Anholt Lab at BMSC

Evolution of sex ratio variation in the copepod Tigriopus californicus

We have been investigating the evolution and ecology of biased sex ratios in the marine copepod Tigriopus californicus. This variation is heritable, and has an environmental component as well. We are currently trying to establish the mechanism by which this occurs.

Dr. Bradley R. Anholt – Principal Investigator

Professor of Biology, University of Victoria
Director, BMSC

Contact:
Email: banholt@uvic.ca
Phone: 250-728-3301
Website

Dr. Heather J. Alexander – Research Associate

Contact:
Email: halexander@bamfieldmsc.com
Phone: 250-728-3301
Website

Erin Hornell – MSc student

Effects of diet on sex ratio of T. californicus

Email: ehornell@uvic.ca

Alumni

Dr. Jean M. L. Richardson – Research Associate

Contact:
Email:  jmlrichardson@gmail.com
Website

Travis Tai – Graduate student (MSc)

Travis tested Fisher’s sex ratio principle (the frequency-dependent evolution of sex ratio) in Tigriopus californicus

Monica Ayala – Graduate student (MSc)

Monica studied host manipulation by parasites in the intertidal snail Littorina sitkana.

Undergraduate students and lab technicians. 

Christine Beulow, AJ Chapelski, Amy MacConnell, Christine Gruman, Shanti Davis, Stephanie Keightley

Michelle van Boven, Phil Lavoie, Andrew Cook, Marie Vance, Tracy MacKeracher, Melissa Macdonald

  • Easily reared in the laboratory; adapted to a harsh high intertidal environment where conditions fluctuate widely.
  • Short generation time; about 21 days at 20°C.
  • Ideal for controlled cross studies: Reproduction occurs year round, and males and virgin females are easily identified. Females only mate once and store sperm, thus all offspring from a single female are full siblings.
  • Populations are genetically subdivided across the geographical range, from Alaska to Baja, California, allowing for the development of population-specific markers the study of  local adaptation.
  • Viable F1 and F2 hybrids despite strong genetic divergence at over long geographical distances, providing the opportunity to study varying degrees of post zygotic isolation.
  • Extensive genetic resources include a range of population-specific markers, genetic linkage map, and fully sequenced genome currently being assembled.

1. Clutch Sex ratio varies among natural populations of Tigriopus californicus.

In Tigriopus californicus, clutch sex ratio variation among families greatly exceeds that expected if sex were determined using a sex chromosome system (Voordouw and Anholt 2002a), and it has long been hypothesized that sex determination in T. californicus is polygenic (Belser 1959).

We sampled T. californicus populations over a two year period to characterize naturally occurring variation in clutch sex ratio among females, within and between geographically isolated locations and over time in Barkley Sound, British Columbia. Because there is some evidence that the environment plays are role in clutch sex ratio (Voordouw and Anholt 2002b), we recorded the temperture in the tidepools where the copepods were sampled from.

Manuscript in prep.

2. Multi-generational response to artificial selection for biased clutch sex ratios in Tigriopus californicus populations.

Alexander, H.J., Richardson, J.M.L. and B.R. Anholt. 2014.  J. Evol. Biol. 2014. 27 (9): 1921-1929.

We tested the polygenic hypothesis of sex determination in the harpacticoid copepod T. californicus using the criterion of response to selection. We report the first multigenerational quantitative evidence that clutch sex ratio responds to artificial selection for male- and female-biased families, and in multiple populations of T. californicus. In the five of six lines that showed a response to selection, realized heritability estimated by multigenerational analysis ranged from 0.24 to 0.58. Divergence of clutch sex ratio between selection lines is rapid, with response to selection detectable within the first four generations of selection.

Figure 1. The mean ( SE) clutch sex ratio for each of six generations of selection for each sampling population and each selected line. Dotted lines connect the mean clutch sex ratio of individuals selected for the next generation to the mean clutch sex ratio of that generation (i.e. response to selection). Where dotted lines appear to be missing it is because selected means and population means are very similar.

Figure 2. Cumulative response to selection (R) vs. cumulative selection differential (S) of mean clutch sex ratio for six generations of selection in three populations. Unfilled symbols = selection lines for female-biased families, filled symbols = selection lines for male-biased families.

3. Sex without sex chromosomes: genetic architecture of multiple loci independently segregating to determine sex ratios in the copepod Tigriopus californicus.

Alexander, H.J., Richarson, J.M.L., Edmands, S. and B.R. Anholt. 2015. J. Evol. Biol. 2015. 28 (12): 2196-2207.

Here we provide the first direct evidence of polygenic sex determination in Tigriopus californicus, a harpacticoid copepod with no heteromorphic sex chromosomes. Using genetically distinct inbred lines selected for male- and female-biased clutches, we generated a genetic map with 39 SNPs across 12 chromosomes. Quantitative trait locus mapping of sex ratio phenotype (the proportion of male offspring produced by an F2 female) in four F2 families revealed six independently segregating quantitative trait loci on five separate chromosomes, explaining 19% of the variation in sex ratios.

Figure 1. Log Posterior Density (LPD) results from qb.scanone() function of the qtlbim package in R. LPD is analogous to typical LOD scores but averages over all unknowns. Dashed horizontal line shows LOD threshold (2.85) calculated from 1000 permutations using scanone() from the qtl package in R, run on genome without chromosome 10 (Chr. 10) split into two QTL. LPD for Chr. 10 shown in inset plot to accommodate its much larger values; dashed vertical gray line in inset plot shows position of split in Chr. 10.

Figure 2. The difference in mean sex ratio phenotype for each marker; homozygote for Aguilar alleles minus homozygote for San Diego alleles. Positive values indicate AG homozygotes tend to be more male biased than SD homozygotes. Negative values indicate AG homozygotes more female biased than SD homozygotes. Each tick on the x-axis represents a marker position. Grey shading delineates chromosomes. Dashed vertical lines indicate estimated QTL positions.

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Alexander, H.J., Richarson, J.M.L., Edmands, S., and B.R. Anholt. 2015. Sex without sex chromosomes; genetic architecture of multiple loci independently segregating to determine sex ratios in the copepod Tigriopus californicus. J. Evol. Biol. 2015 Dec; 28(12): 2196-207.

Alexander, H.J., Richardson, J.M.L. and Anholt, B.R. 2014. Multi-generational response to artificial selection for biased clutch sex ratios in Tigriopus californicus populations. J Evol Biol. 27 (9): 1921-1929.

Bateman, A. W., Vos, M. and Anholt, B. R. 2014. When to defend: Antipredator defenses and the predation sequence. American Naturalist, 183(6): 847-855.

Fisher, J. T., Pasztor, C., Wilson, A., Volpe, J. P., and Anholt, B. R. 2014. Recolonizing sea otters spatially segregate from pinnipeds on the Canadian Pacific coastline: The implications of segregation for species conservation. Biological Conservation, 177: 148–155.

Richardson, J. M. L., Govindarajulu, P., and Anholt, B. R. 2014. Distribution of the disease pathogen Batrachochytrium dendrobatidis in non-epidemic amphibian communities of western Canada. Ecography, 37(9): 883-893.

Fisher, J. T., Anholt, B. R., Bradbury, S., Wheatley, M. and Volpe, J. P. 2013 Spatial segregation of sympatric marten and fishers: the influence of landscapes and species-scapes. Ecography, 36(2): 240-248.

Fisher, J. T., Bradbury, S., Anholt, B. R., Nolan, L., Roy, L., Volpe, J. P. and Wheatley, M. 2013. Wolverines (Gulo gulo luscus) on the Rocky Mountain slopes: natural heterogeneity and landscape alteration as predictors of distribution. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 91(10): 706-716.

Hamilton, P. T., Richardson, J. M. L., and Anholt, B. R. 2012. Daphnia in tadpole mesocosms: trophic links and interactions with Batrachochytrium dendrobatidis. Freshwater Biology, 57(4): 676–683.

Hamilton, P. T., Richardson, J. M. L., Govindarajulu, P., and Anholt, B. R. 2012. Higher temperature variability increases the impact of Batrachochytrium dendrobatidis and shifts interspecific interactions in tadpole mesocosms. Ecology and Evolution, 2(10): 2450-2459.

Kratina, P., LeCraw, R. M., Ingram, T., and Anholt, B. R. 2012. Stability and persistence of food webs with omnivory: Is there a general pattern?. Ecosphere, 3(6).

Fisher, J. T., Anholt, B. R. and Volpe, J. P.  2011. Body mass explains characteristic scales of habitat selection in terrestrial mammals. Ecology and Evolution, 1(4).

Kratina, P., Hammill, E., and Anholt, B. R. 2010. Stronger inducible defences enhance persistence of intraguild prey. Journal of Animal Ecology, 79(5): 993–999.

Hammill, E., Petchey, O. L., and Anholt, B. R. 2010. Predator functional response changed by induced defenses in prey. American Naturalist, 176(6): 723-731.

Hammill, E., Kratina, P., Beckerman, A. P., and Anholt, B. R. 2010. Precise time interactions between behavioural and morphological defences. Oikos, 119(3): 494-499.

Voordouw, M. J.; Anholt, B. R.; Taylor, P. J.; and Hurd, H. 2009. Rodent malaria-resistant strains of the mosquito, Anopheles gambiae, have slower population growth than -susceptible strains. Bmc Evolutionary Biology, 9: 76.

Voordouw, M. J., Stebbins, G., Robinson, H. E., Perrot-Minnot, M., Rigaud, T., and Anholt, B. R. 2008. Genetic variation in the primary sex ratio in populations of the intertidal copepod, Tigriopus californicus, is widespread on Vancouver Island. Evolutionary Ecology Research, 10(7): 1007-1023.

 

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