Evidence of Segregated Spawning in a Single Marine Fish Stock: Sympatric Divergence of Ecotypes in Icelandic Cod?

There is increasing recognition of intraspecific diversity and population structure within marine fish species, yet there is little direct evidence of the isolating mechanisms that maintain it or documentation of its ecological extent. We analyzed depth and temperature histories collected by electronic data storage tags retrieved from 104 Atlantic cod at liberty ≥1 year to evaluate a possible isolating mechanisms maintaining population structure within the Icelandic cod stock. This stock consists of two distinct behavioral types, resident coastal cod and migratory frontal cod, each occurring within two geographically distinct populations. Despite being captured together on the same spawning grounds, we show the behavioral types seem reproductively isolated by fine-scale differences in spawning habitat selection, primarily depth. Additionally, the different groups occupied distinct seasonal thermal and bathymetric niches that generally demonstrated low levels of overlap throughout the year. Our results indicate that isolating mechanisms, such as differential habitat selection during spawning, might contribute to maintaining diversity and fine-scale population structure in broadcast-spawning marine fishes

Original capture locations of Atlantic cod implanted with data storage tags (DSTs) around Iceland.

<p>Insets show the sampling regions in north (N1) and south (S1-S5) Iceland and indicate the number of recovered coastal (C, ○) and frontal (F, <b>▵</b>) individuals originally tagged and released in that area. The bracketed numbers and filled symbols represent individuals for whom spawning information could be extracted from their DST profile. Scale bar within each inset indicates a distance of 10 km.</p

Temperature and depth profiles collected by electronic data storage tags implanted in Atlantic cod.

<p>Examples of one year depth and temperature profiles of frontal (A) and coastal (B) behavioral types of Atlantic cod in Iceland showing in-migration to spawning habitat, time spent at spawning grounds, and out-migration back to feeding grounds in the highlighted areas. Temperature is represented by a red line while depth is represented by a blue one. Periods interpreted as time spent in spawning aggregations was characterized by the highlighted portions with a clear tidal signature between in-migration and out-migration (C). Arrows indicate events interpreted as possible Atlantic cod spawning events as described by Brawn (1961a, b), Rose (1993), and Hutchings et al. (1999).</p

Definition of coastal and frontal behavioral types of Atlantic cod.

<p>Mean (± SE) proportion of daily depth (A) and temperature (B) ranges experienced by individuals tagged with electronic data storage tags (DSTs). Discriminant function analysis (C) performed on the proportion of daily depth and temperature ranges experienced by each individual indicated a clear separation between the coastal (northern: ○; southern: •) and frontal (northern: <b>▵</b>; southern: ▴) behavioral types based upon the proportion of depth and temperature ranges. The visual and DFA classifications of the five individuals represented by a gray circle or triangle could not be reconciled and these individuals were excluded from further analysis. Arrows indicate individuals whose depth and temperature profiles are displayed in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017528#pone-0017528-g002" target="_blank">Fig. 2a</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017528#pone-0017528-g002" target="_blank">2b</a>.</p

Bivariate kernel density estimates of thermal-bathymetric niches occupied during potential spawning activity of Atlantic cod.

<p>Thermal-bathymetric niches occupied during the spawning season as defined as the period between the end of in-migration and outmigration (A, B) and for periods of inferred presence in a spawning aggregation as indicated by the presence of a clear tidal signature during the spawning season (C, D) are presented for southern coastal (A, C) and frontal (B, D) behavioral types in the Icelandic stock of Atlantic cod. Dotted lines enclose the 95^th, 50^th, and 10^th percentiles of the distributions.</p

Bivariate kernel density estimates of seasonal thermal-bathymetric niches occupied by Atlantic cod ecotypes around Iceland.

<p>Dotted lines enclose the 95^th, 50^th, and 10^th percentiles of the distributions.</p

Phenology of migration and spawning of Atlantic cod in Iceland as extrapolated from recovered electronic data storage tags.

<p>Mean (± SE) Julian (A) and degree (B) day for initiating migration and spawning are shown for each Icelandic cod ecotype (NC = north coastal; NF = north frontal; SC = south coastal; SF = south frontal).</p

THE EVOLUTIONARY GENETIC STATUS OF ICELANDIC EELS.

The Iceland population of Anguilla eels contains an elevated frequency of fish with vertebral numbers lower than those typical of European localities. Several distinct hypotheses have been advanced to account for these morphologically atypical fish: for example, they could represent (1) genetically "pure" American expatriates, (2) genetically "pure" European types with ontogenetic abnormalities, or (3) hybrids between American and European forms. Here we critically test these and other possibilities by examining the joint distributions of allozyme markers, mitochondrial DNA markers, and vertebral numbers in Icelandic eels. The particular patterns of association among the genetic and morphological traits demonstrate that the Iceland population includes, in low frequency, the products of hybridization between American and European eels. Approximately 2-4% of the gene pool in the Iceland eel population is derived from American eel ancestry. This hybrid zone is highly unusual in the biological world, because the mating events in catadromous eels presumably take place thousands of kilometers from where the hybrids are observed as maturing juveniles. The molecular data, in conjunction with the geographic distributions, strongly suggest that the differences in migrational behavior and morphology between American and European eels include an important additive genetic component. Evolutionary hypotheses are advanced to account for the original separation of North Atlantic eels into American and European populations, and for the presence of hybrids in Iceland

THE EVOLUTIONARY GENETIC STATUS OF ICELANDIC EELS.

The Iceland population of Anguilla eels contains an elevated frequency of fish with vertebral numbers lower than those typical of European localities. Several distinct hypotheses have been advanced to account for these morphologically atypical fish: for example, they could represent (1) genetically "pure" American expatriates, (2) genetically "pure" European types with ontogenetic abnormalities, or (3) hybrids between American and European forms. Here we critically test these and other possibilities by examining the joint distributions of allozyme markers, mitochondrial DNA markers, and vertebral numbers in Icelandic eels. The particular patterns of association among the genetic and morphological traits demonstrate that the Iceland population includes, in low frequency, the products of hybridization between American and European eels. Approximately 2-4% of the gene pool in the Iceland eel population is derived from American eel ancestry. This hybrid zone is highly unusual in the biological world, because the mating events in catadromous eels presumably take place thousands of kilometers from where the hybrids are observed as maturing juveniles. The molecular data, in conjunction with the geographic distributions, strongly suggest that the differences in migrational behavior and morphology between American and European eels include an important additive genetic component. Evolutionary hypotheses are advanced to account for the original separation of North Atlantic eels into American and European populations, and for the presence of hybrids in Iceland