Rapid sperm length divergence in a polygynandrous passerine: a mechanism of cryptic speciation?

When populations become geographically isolated, they begin to diverge in various traits and at variable rates. The dynamics of such trait divergences are relevant for understanding evolutionary processes such as local adaptation and speciation. Here we examine divergences in sperm and body structures in a polygynandrous songbird, the alpine accentor (Prunella collaris) between two allopatric high-altitude populations, in Morocco and Spain. The populations diverged around 82,000 years ago, as estimated with a coalescence-based phylogenetic analysis of genome-wide single-nucleotide polymorphisms. We found that birds in the two areas had nonoverlapping sperm lengths, which suggests adaptation to divergent female reproductive tract environments. Sperm length also showed an exceptionally low coefficient of among-male variation, a signal of strong stabilizing selection imposed by sperm competition. The evolutionary rate of sperm length was almost twice the rates for the most divergent morphological traits and more than three times higher than expected from literature data over a similar generational timescale. This rapid evolution of a key reproductive trait has implications for reproductive isolation and ultimately for speciation. Strong selection for different sperm length optima in allopatry predicts conspecific sperm precedence and disruptive selection in sympatry, hence a possible postcopulatory prezygotic barrier to gene flow.

Flagellum tapering and midpiece volume in songbird spermatozoa.

In contrast to numerous studies on spermatozoa length, relatively little work focuses on the width of spermatozoa, and particularly the width of the midpiece and flagellum. In flagellated spermatozoa, the flagellum provides forward thrust while energy may be provided via mitochondria in the midpiece and/or through glycolysis along the flagellum itself. Longer flagella may be able to provide greater thrust but may also require stronger structural features and more or larger mitochondria to supply sufficient energy. Here, we use scanning electron microscopy to investigate the ultrastructure of spermatozoa from 55 passerine species in 26 taxonomic families in the Passerides infraorder. Our data confirm the qualitative observation that the flagellum tapers along its length, and we show that longer flagella are wider at the neck. This pattern is similar to mammals, and likely reflects the need for longer cells to be stronger against shearing forces. We further estimate the volume of the mitochondrial helix and show that it correlates well with midpiece length, supporting the use of midpiece length as a proxy for mitochondrial volume, at least in between-species studies where midpiece length is highly variable. These results provide important context for understanding the evolutionary correlations among different sperm cell components and dimensions.

Sperm length divergence as a potential prezygotic barrier in a passerine hybrid zone.

The saltmarsh sparrow Ammospiza caudacuta and Nelson's sparrow A. nelsoni differ in ecological niche, mating behavior, and plumage, but they hybridize where their breeding distributions overlap. In this advanced hybrid zone, past interbreeding and current backcrossing result in substantial genomic introgression in both directions, although few hybrids are currently produced in most locations. However, because both species are nonterritorial and have only brief male-female interactions, it is difficult to determine to what extent assortative mating explains the low frequency of hybrid offspring. Since females often copulate with multiple males, a role of sperm as a postcopulatory prezygotic barrier appears plausible. Here, we show that sperm length differs between the two species in the hybrid zone, with low among-male variation consistent with strong postcopulatory sexual selection on sperm cells. We hypothesize that divergence in sperm length may constitute a reproductive barrier between species, as sperm length co-evolves with the size of specialized female sperm storage tubules. Sperm does not appear to act as a postzygotic barrier, as sperm from hybrids was unexceptional.

Kin selection and polygyny: can relatedness lower the polygyny threshold?

Resource polygyny incurs costs of having to share breeding resources for female breeders. When breeding with a relative, however, such costs may be lessened by indirect fitness benefits through kin selection, while benefits from mutualistic behaviour, such as communal defence, may increase. If so, females should be less resistant to sharing a territory with a related female than with a non-related one. We investigated whether kin selection may lower the threshold of breeding polygynously, predicting a closer relatedness between polygynous females breeding on the same territory than between females breeding on different territories. Northern lapwings, Vanellus vanellus, are suitable for testing this hypothesis as they are commonly polygynous, both sexes take part in nest defence, and the efficiency of nest defence increases with the number of defenders. Using an index of relatedness derived from DNA fingerprinting, we found that female lapwings that shared polygynous dyads were on average twice as closely related as were random females. Furthermore, relatedness did not correlate with distance between breeders, indicating that our findings cannot be explained by natal philopatry alone. Our results suggest that the polygyny threshold in lapwings may be lowered by inclusive fitness advantages of kin selection.

A survey of dioxin-like contaminants in fish from recreational fishing.

The dioxin and dioxin-like compounds are regarded as one of the most toxic group of environmental contaminants. Food for the commercial market is regularly monitored for their dioxin levels and the concentration allowed in food is strictly regulated. Less is known about locally caught fish from recreational fishing, which is often brought home for consumption. This can be fish caught from nearby lakes or streams or fish with marine origin close to industrial areas or harbours that are not regularly monitored for their dioxin levels. In this study, we established collaboration with schools in 13 countries. We received 203 samples of 29 different fish species of which Atlantic cod was the most abundant followed by brown trout and pollock. In general, the majority of samples from the participating countries had low concentrations (between 0.1 and 0.2 pg/g chemical-activated luciferase gene expression toxic equivalency wet weight (CALUX TEQ w.w.)) of dioxins and dioxin-like PCBs. Only 18 samples had concentrations above 1 pg/g CALUX TEQ w.w., and only 2 dab samples had concentration above maximum levels set by the European Commission. The Atlantic cod samples showed a significant reduction in the concentrations of dioxins with increasing latitude indicating less contamination of dioxin and dioxin-like compounds in the north of Norway. The results indicate that a moderate consumption of self-caught fish at presumed non-contaminated sites does not represent a major risk for exposure to dioxins or dioxin-like compounds at concentrations associated with adverse health effects. Recreational fishermen should, however, obtain knowledge about local fish consumption advice.