Tidal gradients, fine-scale homing and a potential cryptic ecotype of wild spawning pink salmon (Oncorhynchus gorbuscha).

The homing behaviour of salmon is a remarkable natural phenomenon, critical for shaping the ecology and evolution of populations yet the spatial scale at which it occurs is poorly understood. This study investigated the spatial scale and mechanisms driving homing as depicted by spawning site-choice behaviour in pink salmon (Oncorhynchus gorbuscha) in Prince William Sound, Alaska. Molecular pedigree analyses of over 30,000 adult spawners in four streams revealed that pink salmon exhibit fine-scale site fidelity within a stream, returning to within <100 m of their parents. Homing behaviours were driven in part by a salinity gradient between intertidal and freshwater environments, with individuals incubated in freshwater environments more than twice as likely to spawn upstream of tidal influence than those incubated in the intertidal. Our findings challenge the traditional view that pink salmon populations are genetically and phenotypically homogenous due to their short freshwater residency as juveniles and high rates of dispersal as returning adults (i.e. straying). This study has important implications for rates of inbreeding, local adaptation and gene flow within populations, and is particularly relevant to the management of salmon hatcheries, given the high incidence of hatchery-origin pink salmon, reared in freshwater hatchery environments, that stray into wild populations of Prince William Sound.

Magnetic maps in animal navigation.

In addition to providing animals with a source of directional or 'compass' information, Earth's magnetic field also provides a potential source of positional or 'map' information that animals might exploit to assess location. In less than a generation, the idea that animals use Earth's magnetic field as a kind of map has gone from a contentious hypothesis to a well-established tenet of animal navigation. Diverse animals ranging from lobsters to birds are now known to use magnetic positional information for a variety of purposes, including staying on track along migratory pathways, adjusting food intake at appropriate points in a migration, remaining within a suitable oceanic region, and navigating toward specific goals. Recent findings also indicate that sea turtles, salmon, and at least some birds imprint on the magnetic field of their natal area when young and use this information to facilitate return as adults, a process that may underlie long-distance natal homing (a.k.a. natal philopatry) in many species. Despite recent progress, much remains to be learned about the organization of magnetic maps, how they develop, and how animals use them in navigation.

Historical DNA documents long-distance natal homing in marine fish.

The occurrence of natal homing in marine fish remains a fundamental question in fish ecology as its unequivocal demonstration requires tracking of individuals from fertilization to reproduction. Here, we provide evidence of long-distance natal homing (>1000 km) over more than 60 years in Atlantic cod (Gadus morhua), through genetic analysis of archived samples from marked and recaptured individuals. Using a high differentiation single-nucleotide polymorphism assay, we demonstrate that the vast majority of cod tagged in West Greenland and recaptured on Icelandic spawning grounds belonged to the Iceland offshore population, strongly supporting a hypothesis of homing. The high degree of natal fidelity observed provides the evolutionary settings for development of locally adapted populations in marine fish and emphasize the need to consider portfolio effects in marine fisheries management strategies.

Evidence that Magnetic Navigation and Geomagnetic Imprinting Shape Spatial Genetic Variation in Sea Turtles.

The canonical drivers of population genetic structure, or spatial genetic variation, are isolation by distance and isolation by environment. Isolation by distance predicts that neighboring populations will be genetically similar and geographically distant populations will be genetically distinct [1]. Numerous examples also exist of isolation by environment, a phenomenon in which populations that inhabit similar environments (e.g., same elevation, temperature, or vegetation) are genetically similar even if they are distant, whereas populations that inhabit different environments are genetically distinct even when geographically close [2-4]. These dual models provide a widely accepted conceptual framework for understanding population structure [5-8]. Here, we present evidence for an additional, novel process that we call isolation by navigation, in which the navigational mechanism used by a long-distance migrant influences population structure independently of isolation by either distance or environment. Specifically, we investigated the population structure of loggerhead sea turtles (Caretta caretta) [9], which return to nest on their natal beaches by seeking out unique magnetic signatures along the coast-a behavior known as geomagnetic imprinting [10-12]. Results reveal that spatial variation in Earth's magnetic field strongly predicts genetic differentiation between nesting beaches, even when environmental similarities and geographic proximity are taken into account. The findings provide genetic corroboration of geomagnetic imprinting [10, 13]. Moreover, they provide strong evidence that geomagnetic imprinting and magnetic navigation help shape the population structure of sea turtles and perhaps numerous other long-distance migrants that return to their natal areas to reproduce [13-17].

Assessing the role of ontogenetic movement in maintaining population structure in fish using otolith microchemistry.

Identifying the mechanisms maintaining population structure in marine fish species with more than a single dispersing life stage is challenging because of the difficulty in tracking all life stages. Here, a two-stage otolith microchemistry approach to examining life-stage movement was adopted, tracking a year-class from the juvenile to adult stage and inferring larval sources from clustering, in order to consider the mechanisms maintaining population structuring in North Sea cod. Clustering of near-core chemistry identified four clusters, two of which had either a southern or northern affinity and were similar to juvenile edge chemistry. The other two clusters, common to the central North Sea, had intermediate chemical composition and may have reflected either larval mixing in this region or a lack of geographic heterogeneity in the elemental signature. From the comparison of whole juvenile and the corresponding component of adult otoliths, adults from the southern North Sea mostly recruited from adjacent nursery grounds. In contrast, many adults in the northern North Sea had a juvenile chemistry consistent with the Skagerrak and juveniles from the northern Skagerrak site had a near-core chemistry consistent with the northern North Sea. Similarities in otolith chemistry were consistent with retention of early life stages at a regional level and also juvenile and adult fidelity. The links between the northern North Sea and Skagerrak indicate natal homing, which when considered in the context of genetic evidence is suggestive of philopatry. The approach used here should be useful in exploring the mechanisms underlying population structuring in other species with multiple dispersive life stages and calcified hard parts.

Natal foraging philopatry in eastern Pacific hawksbill turtles.

The complex processes involved with animal migration have long been a subject of biological interest, and broad-scale movement patterns of many marine turtle populations still remain unresolved. While it is widely accepted that once marine turtles reach sexual maturity they home to natal areas for nesting or reproduction, the role of philopatry to natal areas during other life stages has received less scrutiny, despite widespread evidence across the taxa. Here we report on genetic research that indicates that juvenile hawksbill turtles (Eretmochelys imbricata) in the eastern Pacific Ocean use foraging grounds in the region of their natal beaches, a pattern we term natal foraging philopatry. Our findings confirm that traditional views of natal homing solely for reproduction are incomplete and that many marine turtle species exhibit philopatry to natal areas to forage. Our results have important implications for life-history research and conservation of marine turtles and may extend to other wide-ranging marine vertebrates that demonstrate natal philopatry.

MATRIARCHAL POPULATION GENETIC STRUCTURE IN AN AVIAN SPECIES WITH FEMALE NATAL PHILOPATRY.

We employ mitochondrial (mt) DNA markers to examine the matrilineal component of population genetic structure in the snow goose Chen caerulescens. From banding returns, it is known that females typically nest at their natal or prior nest site, whereas males pair with females on mixed wintering grounds and mediate considerable nuclear gene flow between geographically separate breeding colonies. Despite site philopatry documented for females, mtDNA markers show no clear distinctions between nesting populations across the species' range from Wrangel Island, USSR to Baffin Island in the eastern Canadian Arctic. Two major mtDNA clades (as well as rare haplotypes) are distributed widely and provide one of the few available examples of a phylogeographic pattern in which phylogenetic discontinuity in a gene tree exists without obvious geographic localization within a species' range. The major mtDNA clades may have differentiated in Pleistocene refugia, and colonized current nesting sites through recent range expansion via pulsed or continual low-level dispersal by females. The contrast between results of banding returns and mtDNA distributions in the snow goose raises general issues regarding population structure: direct contemporary observations on dispersal and gene flow can in some cases convey a misleading impression of phylogeographic population structure, because they fail to access the evolutionary component of population connectedness; conversely, geographic distributions of genetic markers can provide a misleading impression of contemporary dispersal and gene flow because they retain a record of evolutionary events and past demographic parameters that may differ from those of the present. An understanding of population structure requires integration of both evolutionary (genetic) and contemporary (direct observational) perspectives.

GLOBAL POPULATION STRUCTURE AND NATURAL HISTORY OF THE GREEN TURTLE (CHELONIA MYDAS) IN TERMS OF MATRIARCHAL PHYLOGENY.

To address aspects of the evolution and natural history of green turtles, we assayed mitochondrial (mt) DNA genotypes from 226 specimens representing 15 major rookeries around the world. Phylogenetic analyses of these data revealed (1) a comparatively low level of mtDNA variability and a slow mtDNA evolutionary rate (relative to estimates for many other vertebrates); (2) a fundamental phylogenetic split distinguishing all green turtles in the Atlantic-Mediterranean from those in the Indian-Pacific Oceans; (3) no evidence for matrilineal distinctiveness of a commonly recognized taxonomic form in the East Pacific (the black turtle C.m. agassizi or C. agassizi); (4) in opposition to published hypotheses, a recent origin for the Ascension Island rookery, and its close genetic relationship to a geographically proximate rookery in Brazil; and (5) a geographic population substructure within each ocean basin (typically involving fixed or nearly fixed genotypic differences between nesting populations) that suggests a strong propensity for natal homing by females. Overall, the global matriarchal phylogeny of Chelonia mydas appears to have been shaped by both geography (ocean basin separations) and behavior (natal homing on regional or rookery-specific scales). The shallow evolutionary population structure within ocean basins likely results from demographic turnover (extinction and colonization) of rookeries over time frames that are short by evolutionary standards but long by ecological standards.