Download What do we know about the genetics of anguillid eels?

What do we know about the
genetics of anguillid eels?
Eric Hallerman
Virginia Polytechnic Institute and State University
H0: Given that all American eels spawn in the
Sargasso Sea, we should expect panmixia.
Is this the case?
•
•
•
•
•
•
•
Williams et al. (1973) examined elvers, juveniles, adults
from FL, NC, NY, NS, NFLD
Screened polymorphic enzyme markers at 5 loci
Found geographic variation in allele frequencies within
life stages
Showed allele frequency differences ~10% among
samples over a 20o latitudinal range
What would we see over the 50o latitudinal range of the
species??
There are no self-sustaining localized populations –
hence, this differentiation must arise anew every
generation!
Clinal SDH and ADH variation in elvers, PHI in adults –
hence, different selective pressures on different life
stages
Williams, G.C., R.K. Koehn, and J.B.
Mitton. 1973. Genetic differentiation
without isolation in the American eel,
Anguilla rostrata. Evolution 27:192204.
•
Koehn and Williams (1978): Are the selective regimes
temporally stable?
•
•
•
•
Elvers and juveniles PR, FL, NY, NS, NFLD various years
Screened for variation at SDH, PHI, ADH loci
Spatial heterogeneity was stable at SDH and PHI loci
Clinal SDH variation was identical in recruits and residents –
hence, selection operated before recruits entered rivers
Clinal PHI variation seen only in residents – hence, selection
operated after recruits took up residence in rivers
Selective pressures at SDH and PHI loci are temporally stable
ADH variation homogeneous across North America, but
varied among years
Selective regimes are dynamic
•
•
•
•
Koehn, R.K., and G.C. Williams.
1978. Genetic differentiation
without isolation in the American
eel, Anguilla rostrata. II. Temporal
stability of geographic patterns.
Evolution 32:624-637.
Williams and Koehn (1984) reviewed the meristics and genetics of A. rostrata
and A. anguilla. Key aspects:
There is no evidence of self-sustaining local populations within putative species
The only genetic evidence for distinct species of Anguilla is from variation at the MDH-2
locus
Intercontinental genetic differentiation is comparable to that observed among conspecific
populations, not distinct species
There is intergradation and gene flow at least from American to European forms:
• Species diagnostic character - number of vertebrae
• Low vertebral counts sometimes seen in Icelandic and Swedish localities
• Icelandic eels have intermediate vertebral counts and MDH alleles from both types
W&K concluded that American and European eels are partially separated breeding
populations of one species, A. anguilla
Skewed sex ratios are often observed:
• Sex determination may have both genetic and environmental components
• Suggested environmental manipulation and common garden experiments
Williams, G.C., and R.K. Koehn. 1984. Population genetics of north Atlantic catadromous eels (Anguilla). Pages
529-560 in B.J. Turner, ed. Evolutionary genetics of fishes. Plenum Press, NY.
Williams, G.C. et al. 1984. Icelandic eels: evidence for a single species of Anguilla in the North Atlantic. Copeia.
•
Avise et al. (1986): Would mtDNA show geographic
variation in North Atlantic eels?
•
•
•
9 sites: LA, FL, GA-2, NC, RI, ME, Ireland, England
Restriction site variation for 14 informative enzymes
A. rostrata homogeneous – one haplotype predominated in
all North American samples; variants differed at 1 or 2
restriction sites; mean divergence p ~0.001
A. anguilla more variable; greater divergence among
haplotypes; mean divergence p ~0.008; no differentiation
between Irish and English populations
Comparison of species: 11 of 14 enzymes showed distinct
digestion profiles. Hence, species very distinct, p ~0.037.
Hypotheses:
•
•
•
• A. rostrata and A. anguilla spawn sympatrically, but do
not interbreed.
• A. rostrata and A. anguilla spawn allopatrically, such that
larval dispersal leads to observed continental distribution
Avise, J.C., et al. 1986.
Mitochondrial DNA
differentiation in north Atlantic
eels: population genetic
consequences of an unusual life
history pattern. Proc. Natl. Acad.
Sci. USA 83:4350-4354.
•
•
•
•
•
•
•
Avise et al. (1988) assumed large population size and
high gene flow within American eel
Estimated time since the most recent common ancestor
on basis of data from Avise et al. (1986)
Molecular distances among mtDNA lineages were small,
2-3 orders of magnitude less than predicted on basis of
current population size
Hypothesis 1: MtDNA evolution is slowed in this species
Hypothesis 2: Long term Nef = 5,500 is much less than
current Ne
With high fecundity (> 1 million eggs), there is great
opportunity for high variance of progeny numbers among
families, decreasing Ne, reducing variability
Ne << N
Avise, J.C., et al. 1988. Current
versus historical population size in
vertebrate species wit high gene flow:
A comparison based on mitochondrial
DNA lineages and inbreeding theory
for neutral mutations. Mol. Biol.
Evol. 5:331-344
•
•
•
•
•
•
•
•
American and European eels differ only in number of
vertebrae and geographic distribution
Are A. rostrata and A. anguilla really distinct species?
What about eels with low vertebral numbers in Iceland
and, rarely, Europe?
Avise et al. (1990) examined eels from four sites in Iceland
for mtDNA, MDH-2, and vertebral counts
Icelandic eels include interspecific hybrids at sites 1 and 2;
hybridization in both directions with regard to sex
Genes are flowing from A. rostrata into A. anguilla
background. 2-4% of gene pool is of American eel
ancestry
Migration behavior and morphology of hybrids
intermediate to parents, suggesting additive genetic mode
of expression
Authors hypothesize that all Atlantic eels one derive from
a single population that became separated into two forms
~1.5 mya; divergent gene pools arose and maintained by
disruptive selection for larval development rate and by
spawning in separate areas of the Sargasso Sea
Avise, J.C, et al. 1990. The
evolutionary genetic status of
Icelandic eels. Evolution
44:1254-1262.
Can we learn anything pertinent
from studies of other anguillid
eels?
• Japanese eel, A. japonica
•
Neither isozymes nor mitochondrial DNA show
geographic genetic differentiation
•
Taniguchi, N., and K. Numachi. 1978. Genetic variation of 6PGDH, IDH, and
GOT in the liver of Japanese eel. Bull. Jpn. Soc. Sci. Fish.44:1351-1355.
Song et al. 1994. Population structure of the Japanese eels, Anguilla japonica.
Molecular Biology and Evolution 11:250-260.
•
Can we learn anything pertinent from
studies of other anguillid eels?
• European eel, A.anguilla
•
Allozymes – no evidence against hypothesis of panmixia:
•
DeLigny, W., and E.M. Pantelouris. 1973. Origin of the European eel. Nature 246:518519.
Comparini, A.., et al. 1977. Genetic control and variability of phosphoglucose isomerase
(PGI) in eels of the Atlantic Ocean and the Mediterranean Sea. Mar. Biol. 43:109-116.
Rodino, E., and A. Comparini. 1978. Genetic variability in the European eel, Anguilla
anguilla L. in Battaglia and Beardmore, eds. Marine organisms: Genetics, ecology, and
evolution. Plenum Press, NY.
•
•
•
But variation is clinal:
•
Pantelouris, E.M., et al. 1970. Genetic variation in the eel. Genet. Res. Camb. 16277284.
•
MtDNA – no evidence against hypothesis of panmixia:
•
Lintas C., et al. 1998. Genetic variation in the European eel (Anguilla anguilla). Mol.
Mar. Biol. Biotech. 7:263-269.
Can we learn anything pertinent from studies
of other anguillid eels?
•
•
•
•
•
•
•
•
Microsatellite DNA
Wirth and Bernatchez (2001) examined variation at 7
microsatellite loci among 13 populations from north
Atlantic, Baltic Sea, Mediterranean Sea
13-21 alleles per locus
There was weak but significant genetic differentiation (FST
= 0.0017), especially of Mediterranean vs. Baltic and
North Sea populations
Significant correlation with distance
Authors suggest stocks are maintained by spawners
arriving at different times at spawning areas and larval
homing (tenuous?)
Authors did not consider effect of selection occurring after
larval dispersal as in A. rostrata
Note that differentiation was observed only with powerful
microsatellite markers
Wirth, T., and L. Bernatchez.
2001. Genetic evidence against
panmixia in the European eel.
Nature 409:1037-1040.
Research questions relevant to management
of A. rostrata: Genetic issues
• What is genetic variation across the
entire range of A. rostrata from
Surinam to Greenland?
• Would screening of microsatellite
DNA markers reveal new findings?
• The A. anguilla microsatellite primers would
probably work for A. rostrata
What if we find geographic genetic variation?
•
•
•
Case study: Salmonids
Many offshore fisheries are actually
mixtures of distinct spawning
populations
Ex: Chinook salmon troll fishery
Miller, M., et al. 1983. Analysis of chinook stock
composition in the May 1982 troll fishery off the Washington
coast: an application of the genetic stock identification
method. Washington States Dept. of Fisheries Technical
Rept. No 74. 27 pp.
What if we find geographic genetic variation?
• The most likely composition of a mixed stock fishery can be
estimated:
Milner, G.B., et al. 1985. A genetic method of stock
identification in mixed populations of Pacific salmon,
Oncorhynchus sp. Mar. Fish. Rev. 47:1-8.
What if we find geographic genetic variation?
Harvest is managed so
as to protect the
demographically most
vulnerable population(s)
Miller, M., et al. 1983. Analysis of chinook stock
composition in the May 1982 troll fishery off the
Washington coast: an application of the genetic stock
identification method. Washington States Dept. of
Fisheries Technical Rept. No 74. 27 pp.
Research questions relevant to management
of A. rostrata: Ecological -demographic
issues
• Are population trends similar for both American and European
eels (perhaps with a 1-2 year lag)? How would the answer
affect inference of causal factors?
• Could the apparent decline of North American eels be due in
part to harvest of elvers for aquaculture?