Thresholds for adding degraded tropical forest to the conservation estate.

Logged and disturbed forests are often viewed as degraded and depauperate environments compared with primary forest. However, they are dynamic ecosystems1 that provide refugia for large amounts of biodiversity2,3, so we cannot afford to underestimate their conservation value4. Here we present empirically defined thresholds for categorizing the conservation value of logged forests, using one of the most comprehensive assessments of taxon responses to habitat degradation in any tropical forest environment. We analysed the impact of logging intensity on the individual occurrence patterns of 1,681 taxa belonging to 86 taxonomic orders and 126 functional groups in Sabah, Malaysia. Our results demonstrate the existence of two conservation-relevant thresholds. First, lightly logged forests (<29% biomass removal) retain high conservation value and a largely intact functional composition, and are therefore likely to recover their pre-logging values if allowed to undergo natural regeneration. Second, the most extreme impacts occur in heavily degraded forests with more than two-thirds (>68%) of their biomass removed, and these are likely to require more expensive measures to recover their biodiversity value. Overall, our data confirm that primary forests are irreplaceable5, but they also reinforce the message that logged forests retain considerable conservation value that should not be overlooked.

Transcriptomics of differences in thermal plasticity associated with selection for an exaggerated male sexual trait.

The information about the magnitude of differences in thermal plasticity both between and within populations, as well as identification of the underlying molecular mechanisms are key to understanding the evolution of thermal plasticity. In particular, genes underlying variation in the physiological response to temperature can provide raw material for selection acting on plastic traits. Using RNAseq, we investigate the transcriptional response to temperature in males and females from bulb mite populations selected for the increased frequency of one of two discrete male morphs (fighter- and scrambler-selected populations) that differ in relative fitness depending on temperature. We show that different mechanisms underlie the divergence in thermal response between fighter- and scrambler-selected populations at decreased vs. increased temperature. Temperature decrease to 18 °C was associated with higher transcriptomic plasticity of males with more elaborate armaments, as indicated by a significant selection-by-temperature interaction effect on the expression of 40 genes, 38 of which were upregulated in fighter-selected populations in response to temperature decrease. In response to 28 °C, no selection-by-temperature interaction in gene expression was detected. Hence, differences in phenotypic response to temperature increase likely depended on genes associated with their distinct morph-specific thermal tolerance. Selection of males also drove gene expression patterns in females. These patterns could be associated with temperature-dependent fitness differences between females from fighter- vs. scrambler-selected populations reported in previous studies. Our study shows that selection for divergent male sexually selected morphologies and behaviors has a potential to drive divergence in metabolic pathways underlying plastic response to temperature in both sexes.

Sexual selection predicts the persistence of populations within altered environments.

The effect of sexual selection on species persistence remains unclear. The cost of bearing ornaments or armaments might increase extinction risk, but sexual selection can also enhance the spread of beneficial alleles and increase the removal of deleterious alleles, potentially reducing extinction risk. Here we investigate the effect of sexual selection on species persistence in a community of 34 species of dung beetles across a gradient of environmental disturbance ranging from old growth forest to oil palm plantation. Horns are sexually selected traits used in contests between males, and we find that both horn presence and relative size are strongly positively associated with species persistence and abundance in altered habitats. Testes mass, an indicator of post-copulatory selection, is, however, negatively linked with the abundance of species within the most disturbed habitats. This study represents the first evidence from a field system of a population-level benefit from pre-copulatory sexual selection.

The effect of sexual selection on adaptation and extinction under increasing temperatures.

Strong sexual selection has been reported to both enhance and hinder the adaptive capacity and persistence of populations when exposed to novel environments. Consequently, how sexual selection influences population adaption and persistence under stress remains widely debated. Here, we present two empirical investigations of the fitness consequences of sexual selection on populations of the Indian meal moth, Plodia interpunctella, exposed to stable or gradually increasing temperatures. When faced with increasing temperatures, strong sexual selection was associated with both increased fecundity and offspring survival compared with populations experiencing weak sexual selection, suggesting sexual selection acts to drive adaptive evolution by favouring beneficial alleles. Strong sexual selection did not, however, delay extinction when the temperature became excessively high. By manipulating individuals' mating opportunities during fitness assays, we were able to assess the effect of multiple mating independently from the effect of population-level sexual selection, and found that polyandry has a positive effect on both fecundity and offspring survival under increasing temperatures in those populations evolving with weak sexual selection. Within stable temperatures, there were some benefits from strong sexual selection but these were not consistent across the entire experiment, possibly reflecting changing costs and benefits of sexual selection under stabilizing and directional selection. These results indicate that sexual selection can provide a buffer against climate change and increase adaptation rates within a continuously changing environment. These positive effects of sexual selection may, however, be too small to protect populations and delay extinction when environmental changes are relatively rapid.

Sperm morph and remating frequency in the Indian meal moth, Plodia interpunctella.

All Lepidoptera produce two sperm types: normal, nucleated 'eupyrene' sperm and anucleate 'apyrene' sperm. One hypothesis for the evolution of apyrene sperm suggests that they act to reduce female remating rate. Apyrene sperm require less resources to produce than do eupyrene sperm, and could delay remating by females by acting as a 'cheap filler', packing the spermatheca and thereby reducing receptivity. This would reduce the risk of sperm competition, giving a potential adaptive advantage to the male producing these sperm. This leads to the prediction that the probability of a female remating should correlate with the number of stored apyrene sperm, which has previously been supported by experiments using the green-veined white butterfly, Pieris napi We repeated this experiment using the Indian meal moth, Plodia interpunctella We find that in this species, eupyrene, not apyrene sperm number is the best predictor of female remating probability, indicating that the 'cheap filler' hypothesis for the function of apyrene sperm is not well supported in Pl. interpunctella.

Alternative reproductive tactics and evolutionary rescue.

Almost all life on earth is facing environmental change, and understanding how populations will respond to these changes is of urgent importance. One factor that is known to affect the speed by which a population can evolve when faced with changes in the environment is strong sexual selection. This increases the adaptive capacity of a population by increasing reproductive skew toward well-adapted (usually) males who will, on average, be best able to compete for matings. This effect could potentially be disrupted when males pursue alternative reproductive tactics (ARTs), whereby males within a species exhibit qualitatively different behaviors in their pursuit of matings. ARTs are diverse, but one common class is those expressed through condition-dependent polyphenism such that high-quality, well-adapted males compete aggressively for mates and low-quality, poorly adapted males attempt to acquire matings via other, nonaggressive behaviors. Here, using an individual-based modeling approach, we consider the possible impacts of ARTs on adaptation and evolutionary rescue. When the ART is simultaneous, meaning that low-quality males not only engage in contests but also pursue other tactics, adaptive capacity is reduced and evolutionary rescue, where a population avoids extinction by adapting to a changing environment, becomes less likely. This is because the use of the ART allows low-quality males to contribute more maladaptive genes to the population than would happen otherwise. When the ART is fixed, however, such that low-quality males will only use the alternative tactic and do not engage in contests, we find the opposite: adaptation happens more quickly and evolutionary rescue when the environment changes is more likely. This surprising effect is caused by an increase in the mating success of the highest quality males who face many fewer competitors in this scenario-counterintuitively, the presence of males pursuing the ART increases reproductive skew toward those males in the best condition.

Sexually selected male weapon increases the risk of population extinction under environmental change: an experimental evidence.

Exaggerated sexually selected traits (SSTs), occurring more commonly in males, help individuals to increase reproductive success but are costly to produce and maintain. These costs on the one hand may improve population fitness by intensifying selection against maladapted males, but on the other hand, may increase the risk of extinction under environmental challenges. However, the impact of SSTs on extinction risk has not been investigated experimentally. We used replicate populations of a male-dimorphic mite, Rhizoglyphus robini, to test if the prevalence of a sexually selected weapon affected the risk of extinction under temperature increase (TI) (2°C per each of three consecutive generations). In two independent experiments that utilized either inbred lines or lines mass selected for or against the weapon to establish experimental replicate populations differing in the prevalence of the weapon, we found that populations with high weapon prevalence were more likely to go extinct. Extinctions occurred despite partial suppression of the weapon expression at increased temperature and were not explained by increased male mortality. Our results provide the first, to our knowledge, experimental evidence demonstrating the dramatic effect of elaborated sexual traits on the risk of extinction under environmental challenges.

A sexually selected male weapon characterized by strong additive genetic variance and no evidence for sexually antagonistic polyphenic maintenance.

Sexual selection and sexual antagonism are important drivers of eco-evolutionary processes. The evolution of traits shaped by these processes depends on their genetic architecture, which remains poorly studied. Here, implementing a quantitative genetics approach using diallel crosses of the bulb mite, Rhizoglyphus robini, we investigated the genetic variance that underlies a sexually selected weapon that is dimorphic among males and female fecundity. Previous studies indicated that a negative genetic correlation between these two traits likely exists. We found male morph showed considerable additive genetic variance, which is unlikely to be explained solely by mutation-selection balance, indicating the likely presence of large-effect loci. However, a significant magnitude of inbreeding depression also indicates that morph expression is likely to be condition-dependent to some degree and that deleterious recessives can simultaneously contribute to morph expression. Female fecundity also showed a high degree of inbreeding depression, but the variance in female fecundity was mostly explained by epistatic effects, with very little contribution from additive effects. We found no significant genetic correlation, nor any evidence for dominance reversal, between male morph and female fecundity. The complex genetic architecture underlying male morph and female fecundity in this system has important implications for our understanding of the evolutionary interplay between purifying selection and sexually antagonistic selection.

Genomic evidence that a sexually selected trait captures genome-wide variation and facilitates the purging of genetic load.

The evolution of costly traits such as deer antlers and peacock trains, which drove the formation of Darwinian sexual selection theory, has been suggested to both reflect and affect patterns of genetic variance across the genome, but direct tests are missing. Here, we used an evolve and resequence approach to reveal patterns of genome-wide diversity associated with the expression of a sexually selected weapon that is dimorphic among males of the bulb mite, Rhizoglyphus robini. Populations selected for the weapon showed reduced genome-wide diversity compared to populations selected against the weapon, particularly in terms of the number of segregating non-synonymous positions, indicating enhanced purifying selection. This increased purifying selection reduced inbreeding depression, but outbred female fitness did not improve, possibly because any benefits were offset by increased sexual antagonism. Most single nucleotide polymorphisms (SNPs) that consistently diverged in response to selection were initially rare and overrepresented in exons, and enriched in regions under balancing or relaxed selection, suggesting they are probably moderately deleterious variants. These diverged SNPs were scattered across the genome, further demonstrating that selection for or against the weapon and the associated changes to the mating system can both capture and influence genome-wide variation.