Incorporating putatively neutral and adaptive genomic data into marine conservation planning

The availability of genomic data for an increasing number of species makes it possible to incorporate evolutionary processes into conservation plans. Recent studies show how genetic data can inform spatial conservation prioritization (SCP), but they focus on metrics of diversity and distinctness derived primarily from neutral genetic data sets. Identifying adaptive genetic markers can provide important information regarding the capacity for populations to adapt to environmental change. Yet, the effect of including metrics based on adaptive genomic data into SCP in comparison to more widely used neutral genetic metrics has not been explored. We used existing genomic data on a commercially exploited species, the giant California sea cucumber (Parastichopus californicus), to perform SCP for the coastal region of British Columbia (BC), Canada. Using a RAD-seq data set for 717 P. californicus individuals across 24 sampling locations, we identified putatively adaptive (i.e., candidate) single nucleotide polymorphisms (SNPs) based on genotype–environment associations with seafloor temperature. We calculated various metrics for both neutral and candidate SNPs and compared SCP outcomes with independent metrics and combinations of metrics. Priority areas varied depending on whether neutral or candidate SNPs were used and on the specific metric used. For example, targeting sites with a high frequency of warm-temperature-associated alleles to support persistence under future warming prioritized areas in the southern coastal region. In contrast, targeting sites with high expected heterozygosity at candidate loci to support persistence under future environmental uncertainty prioritized areas in the north. When combining metrics, all scenarios generated intermediate solutions, protecting sites that span latitudinal and thermal gradients. Our results demonstrate that distinguishing between neutral and adaptive markers can affect conservation solutions and emphasize the importance of defining objectives when choosing among various genomic metrics for SCP.     

Alarming decline of freshwater trigger species in western Mediterranean key biodiversity areas

Theidentification of key biodiversity areas (KBA) was initiated by the International Union for Conservation of Nature in 2004 to overcome taxonomic biases in the selection of important areas for conservation, including freshwater ecosystems. Since then, several KBAs have been identified mainly based on the presence of trigger species (i.e., species that trigger either the vulnerability and or the irreplaceability criterion and thus identify a site as a KBA). However, to our knowledge, many of these KBAs have not been validated. Therefore, classical surveys of the taxa used to identify freshwater KBAs (fishes, molluscs, odonates, and aquatic plants) were conducted in Douro (Iberian Peninsula) and Sebou (Morocco) River basins in the Mediterranean Biodiversity Hotspot. Environmental DNA analyses were undertaken in the Moroccan KBAs. There was a mismatch between the supposed and actual presence of trigger species. None of the trigger species were found in 43% and 50% of all KBAs surveyed in the Douro and Sebou basins, respectively. Shortcomings of freshwater KBA identification relate to flawed or lack of distribution data for trigger species. This situation results from a misleading initial identification of KBAs based on poor (or even inaccurate) ecological information or due to increased human disturbance between initial KBA identification and the present. To improve identification of future freshwater KBAs, we suggest selecting trigger species with a more conservative approach; use of local expert knowledge and digital data (to assess habitat quality, species distribution, and potential threats); consideration of the subcatchment when delineating KBAs boundaries; thoughtful consideration of terrestrial special areas for conservation limits; and periodic field validation.     

Extra-pair paternity in alpine marmots, <Emphasis Type="Italic">Marmota marmota</Emphasis>: genetic quality and genetic diversity effects

Assuming that a male’s genetic characteristics affect those of his offspring, extra-pair copulation has been hypothesized to increase heterozygosity of the progeny—the “genetic compatibility” hypothesis—and the genetic diversity within litters—the “genetic diversity” hypothesis. We tested these two hypotheses in the alpine marmot (Marmota marmota), a socially monogamous mammal showing a high rate of extra-pair paternity (EPP). In a first step, we tested the assumption that a male’s genetic characteristics (heterozygosity and genetic similarity to the female) affect those of his offspring. Genetic similarity between parents influenced offspring heterozygosity, offspring genetic similarity to their mother, and litter genetic diversity. The father’s heterozygosity also influenced litter genetic diversity but did not affect offspring heterozygosity. Hence, heterozygosity seems not to be heritable in the alpine marmot. In a second step, we compared genetic characteristics of extra-pair young (EPY) and within-pair young (WPY). EPY were less genetically similar to their mother but not more heterozygous than WPY. EPY siblings were also less genetically similar than their WPY half siblings. Finally, the presence of EPY promoted genetic diversity within the litter. Thus, our data support both the “genetic compatibility” and the “genetic diversity” hypotheses. We discuss further investigations needed to determine the primary causes of EPP in this species.     

Assessment of patch quality by ladybirds: relative response to conspecific and heterospecific larval tracks a consequence of habitat similarity?

Summary. Aphid colonies can reach high levels of abundance but last for short periods of time. The larvae of aphidophagous ladybirds (Coleoptera: Coccinellidae) that feed on these colonies might therefore suffer from starvation, which favours the occurrence of cannibalism and intraguild predation. Thus, the assessment of patch quality becomes crucial and it has been shown that female ladybirds refrain from laying eggs in the presence of an oviposition deterring semiochemical deposited by their larvae. Adalia bipunctata (L.), Adalia decempunctata (L.) and Coccinella septempunctata L. are 3 sympatric species of ladybirds, which can co-occur in aphid colonies. As a consequence, their eggs and larvae are under threat, not only from cannibalism but also intraguild predation. Females should, therefore, also use the tracks deposited by heterospecific larvae to assess the quality of aphid colonies as oviposition sites. The expectation is that: 1- the strength of the reaction to each other’s larval tracks should be correlated with percentage habitat overlap and that 2- the reaction to conspecific larval tracks should be stronger than to heterospecific tracks. In order to test these hypotheses, females’ oviposition behaviour was analysed and a chemical analysis of the tracks of their larvae undertaken. The results show that oviposition behaviour is not related to habitat overlap. Both species of Adalia react to tracks of their own larvae and those of C. septempunctata, but A. decempunctata reacted more strongly than A. bipunctata. C. septempunctata reacted very slightly to its own tracks but not to those of either species of Adalia. The larval tracks are mainly composed of alkanes. Those of the two species of Adalia are qualitatively 100% similar and 60% so when the quantitative results are compared. They are, however, only 24–29% similar to those of Coccinella septempunctata.     

Seasonal variation in movement,aggregation and destructive grazing of the green sea urchin (<Emphasis Type="Italic">Strongylocentrotus droebachiensis</Emphasis>) in relation to wave action and sea temperature

Hydrodynamic forces are an important determinant of subtidal community structure, particularly when they limit the distribution and foraging ability of mobile consumers. We examined the effect of wave action on the rate of movement and destructive grazing of a kelp bed by the green sea urchin (Strongylocentrotus droebachiensis) under field conditions. We measured density and rate of advance at fixed intervals along ∼100 m of a grazing front over 1 year, and quantified individual movement rates in the barrens 5–10 m behind the urchin front using a time-lapse videography. Seasonal variation in the mean rate of advance of the front (range: 0–4 m month⁻¹) was explained by changes in urchin density at the front (120–360 individuals m⁻²), which in turn varied inversely with significant wave height (0.5–2 m). Water temperature (0.8–17.6°C) had no effect on the rate of advance or on urchin density (aggregation) at the front, except when temperature exceeded 17°C. Movement of individual urchins also was affected by wave action: we observed a significant decrease in speed and displacement of urchins with increasing significant wave height. Wave action had no effect on the proportion of urchins moving or the degree of linearity of their movements. We propose that the decrease in urchin density at the front associated with increased wave action, results from de-aggregation, which reduces the risk of dislodgement, combined with a reduction in urchin movement in barrens, which supplies new urchins to the front.     

Mating system and individual reproductive success of sympatric anadromous and resident brook charr, <Emphasis Type="Italic">Salvelinus fontinalis</Emphasis>, under natural conditions

Salmonids are known for the occurrence in sympatry of two life-history forms, one that undergoes migration to sea before returning to freshwater to reproduce (anadromous) and one that inhabits freshwater without a migration phase (resident). Whereas one breeding population is often suggested by population genetic studies, mating patterns have rarely been directly assessed, especially when both sexes are found within each life-history form. By using highly polymorphic microsatellite loci and parentage analysis in a natural population of sympatric anadromous and resident brook charr (Salvelinus fontinalis), we found that gene flow occurred between the two forms and was mediated by resident males mating with both resident and anadromous females. Determinants of reproductive success, estimated by the number of surviving juveniles (ages 1 and 2 years), differed between the sexes. No strong evidence of the influence of size on individual reproductive success was found for males, whereas larger females (and hence most likely to be anadromous) were more successful. The higher individual reproductive success of anadromous fish compared to residents was mainly explained by this higher reproductive success of anadromous females. We suggest that resident males adopt a “sneaking” reproductive tactic as a way of increasing their reproductive success by mating with females of all sizes in all habitats. The persistence of the resident tactic among females may be linked to their advantage in accessing spatially constrained spawning areas in small tributary streams unavailable to larger females.     

Diving behaviour of Little Penguins from four colonies across their whole distribution range: bathymetry affecting diving effort and fledging success

Little Penguins, Eudyptula minor, breed in several small colonies in New Zealand and Australia. In this study, we compare the birds’ diving performances at different sites situated throughout their breeding range. Environmental conditions and breeding success vary drastically amongst colonies, but all birds feed on similar types of prey and face similar limitations on their foraging range. We examined several diving parameters and calculated the proportion of foraging zone available during breeding to examine whether oceanographic and geographic factors in the foraging zone can explain variations in diving behaviour and fledging success among the different colonies. In colonies with high fledging success, Penguin Island and Oamaru, penguins made shallow dives <50 m depth and had lower diving effort. More than 90% of the foraging zone was in waters <50 m depth in these colonies. Motuara Island also has shallow waters with 95% <50 m depth, but the fledging success was low. Phillip Island has only 42% of waters <50 m and comparatively low fledging success. Thus, penguins dived deeper and showed a higher diving effort in colonies with lower fledging success (Motuara Island and Phillip Island), indicating that they were disadvantaged compared to conspecifics from other colonies that dived shallower and with a lesser diving effort. We concluded that bathymetry is an important factor, but not the only one, which influences fledging success.     

Carotenoid-based colouration and ultraviolet reflectance of the sexual ornaments of grouse

Among the most familiar sexual signals are red, yellow, and orange sexual traits pigmented by carotenoids. Many birds can detect near-ultraviolet (UV) light, and UV signals can play key roles in mate choice. Grouse (Tetraonidae) exhibit bright carotenoid-dependent sexual ornaments, their supra-orbital combs, which to humans appear orange-red. Combs also reflect in the UV, which is not visible to humans but is likely to be visible to grouse. In male red grouse Lagopus lagopus scoticus, we show that comb UV reflectance decreases with increasing comb size and redness. By removing the epidermis of combs, where carotenoid pigments are, we show that the UV reflectance is a property of the dermis, underneath the red pigmented epidermis. Carotenoid pigmentation of combs acted as a mask to reduce reflectance by the dermis in the range 400–550 nm and in the UV, 300–400 nm. Patagium skin (non-ornamental skin under the wing) also reflects in the UV, but epidermis removal on this bare part tended to reduce UV reflectance, whereas removal of the red epidermis of combs increased UV reflectance. Males in better condition (greater body mass relative to size) had bigger and redder combs, but with less UV. Thus, carotenoid pigments of grouse combs are deposited on a white background with significant UV reflectance, which can influence how the signal is perceived by conspecifics. Carotenoid-based traits exhibit UV reflectance in a number of species, but how UV reflectance and carotenoid pigmentation influence colour remains little known for integumentary ornaments compared to plumage traits. UV vision is not uncommon in birds and other animals, so future studies should investigate how UV reflectance influences the perception of carotenoid-based signals of quality.     

Environmental conditions influence egg color of reed warblers <Emphasis Type="Italic">Acrocephalus scirpaceus</Emphasis> and their parasite,the common cuckoo <Emphasis Type="Italic">Cuculus canorus</Emphasis>

The outer layer of the eggshell in birds is in many cases covered by pigments that are assumed to be genetically determined traits with a negligible environmental component. To test the hypothesis that spring environmental conditions (i.e., temperature and rainfall) may affect bird egg pigmentation, we measured by spectrophotometry and photography egg coloration and spottiness on reed warbler (Acrocephalus scirpaceus L.) clutches parasitized by the common cuckoo (Cuculus canorus L.) collected over a period of 24 years and preserved in the Zoological Museum, Copenhagen, Denmark. In addition, we investigated whether spring environmental conditions may influence the coevolutionary relationship between the cuckoo and its host via changes in cuckoo–host egg matching. Generalized mixed models revealed that reed warbler eggs were more brilliant in those springs with a higher rainfall and tended to be bluer and greener in springs with a lower relative temperature. On the other hand, cuckoo eggs were bluer and greener in springs with a higher rainfall. Cuckoo–host egg matching in blue-greenness and spottiness was better in springs with a higher rainfall. These results provide support for the existence of an environmental component on bird egg coloration and suggest that environmental factors may potentially affect the outcome of important features of the arms race between cuckoos and reed warblers.     

Flexible defense strategies: competition modifies investment in behavioral vs. morphological defenses

Competition is predicted to affect the expression of inducible defenses, but because costs of behavioral and morphological antipredator defenses differ along resource gradients, its effects on defenses may depend on the traits considered. We tested the predictions from different defense models in tadpoles of the common frog Rana temporaria, which exhibit both types of defenses. In an outdoor experiment, we exposed the tadpoles to nonlethal predators (Aeshna dragonfly larvae) and to a gradient of intraspecific competition. Morphological responses did not follow any of the expected patterns, since investment in defense was not affected by resource level. Instead, tail depth decreased in the absence of predators. Behavioral defenses followed a state-dependent model. Overall, the defense strategy of the tadpoles revealed a shift from morphological and behavioral defenses at low tadpole density to morphological defense only at high density. This difference probably reflects the different efficiency of the defenses. Hiding is an effective means of defense, but it is unsustainable when resources are scarce. Morphological responses become more important with increasing density to compensate for the increase in behavioral risk-taking. Our results indicate that competition can strongly affect reaction norms of inducible defenses and highlight the importance of integrating ecological parameters that affect the cost-benefit balance of phenotypic plasticity.