Intercontinental genomic parallelism in multiple three-spined stickleback adaptive radiations.

Parallelism, the evolution of similar traits in populations diversifying in similar conditions, provides strong evidence of adaptation by natural selection. Many studies of parallelism focus on comparisons of different ecotypes or contrasting environments, defined a priori, which could upwardly bias the apparent prevalence of parallelism. Here, we estimated genomic parallelism associated with components of environmental and phenotypic variation at an intercontinental scale across four freshwater adaptive radiations (Alaska, British Columbia, Iceland and Scotland) of the three-spined stickleback (Gasterosteus aculeatus). We combined large-scale biological sampling and phenotyping with restriction site associated DNA sequencing (RAD-Seq) data from 73 freshwater lake populations and four marine ones (1,380 fish) to associate genome-wide allele frequencies with continuous distributions of environmental and phenotypic variation. Our three main findings demonstrate that (1) quantitative variation in phenotypes and environments can predict genomic parallelism; (2) genomic parallelism at the early stages of adaptive radiations, even at large geographic scales, is founded on standing variation; and (3) similar environments are a better predictor of genome-wide parallelism than similar phenotypes. Overall, this study validates the importance and predictive power of major phenotypic and environmental factors likely to influence the emergence of common patterns of genomic divergence, providing a clearer picture than analyses of dichotomous phenotypes and environments.

Prior exposure to long-day photoperiods alters immune responses and increases susceptibility to parasitic infection in stickleback.

Seasonal disease and parasitic infection are common across organisms, including humans, and there is increasing evidence for intrinsic seasonal variation in immune systems. Changes are orchestrated through organisms' physiological clocks using cues such as day length. Ample research in diverse taxa has demonstrated multiple immune responses are modulated by photoperiod, but to date, there have been few experimental demonstrations that photoperiod cues alter susceptibility to infection. We investigated the interactions among photoperiod history, immunity and susceptibility in laboratory-bred three-spined stickleback (a long-day breeding fish) and its external, directly reproducing monogenean parasite Gyrodactylus gasterostei. We demonstrate that previous exposure to long-day photoperiods (PLD) increases susceptibility to infection relative to previous exposure to short days (PSD), and modifies the response to infection for the mucin gene muc2 and Treg cytokine foxp3a in skin tissues in an intermediate 12 L : 12 D photoperiod experimental trial. Expression of skin muc2 is reduced in PLD fish, and negatively associated with parasite abundance. We also observe inflammatory gene expression variation associated with natural inter-population variation in resistance, but find that photoperiod modulation of susceptibility is consistent across host populations. Thus, photoperiod modulation of the response to infection is important for host susceptibility, highlighting new mechanisms affecting seasonality of host-parasite interactions.

Internal embryonic development in a non-copulatory, egg-laying teleost, the three-spined stickleback, Gasterosteus aculeatus.

The switch from egg-laying to retaining and giving birth to live young is a major transition in the history of life. Despite its repeated evolution across the fishes, records of intermediate phenotypes are vanishingly rare, with only two known cases in existence of normally egg-laying fish species retaining embryos within the ovaries. We report the discovery of a third occurrence, in which well-developed embryos were found in the ovaries of a three-spined stickleback (Gasterosteus aculeatus), a non-copulatory, normally oviparous species. Extracted from the parent fish, these embryos hatched and grew to adulthood. Genetic and physiological examination of the parent fish and offspring ruled out development by parthenogenesis and hermaphroditism, therefore implicating internal fertilisation by a male stickleback. This extremely rare phenomenon may have been facilitated in this population by an unusual tendency for females to become egg-bound, and suggests that some major transitions may arise almost spontaneously.