Ryan Calsbeek

Sexually Antagonistic Selection, Sexual Dimorphism, and the Resolution of Intralocus Sexual Conflict

Males and females share most of their genomes and express many of the same traits, yet the sexes often have markedly different selective optima for these shared traits. This sexually antagonistic (SA) selection generates intralocus sexual conflict that is thought to be resolved through the evolution of sexual dimorphism. However, we currently know little about the prevalence of SA selection, the components of fitness that generate sexual antagonism, or the relationship between sexual dimorphism and current SA selection. We reviewed published studies to address these questions, using 424 selection estimates representing 89 traits from 34 species. Males and females often differed substantially in the direction and magnitude of selection on shared traits, although statistically significant SA selection was relatively uncommon. Sexual selection generated stronger sexual antagonism than fecundity or viability selection, and these individual components of fitness tended to reinforce one another to generate even stronger sexual antagonism for net fitness. Traits exhibiting strong sexual dimorphism exhibited greater SA selection than did weakly dimorphic traits, although this pattern was not significant after we controlled for the inclusion of multiple traits nested within species. Our results suggest that intralocus sexual conflict often may persist despite the evolution of sexual dimorphism.

Patterns of molecular evolution and diversification in a biodiversity hotspot: The California Floristic Province

The California Floristic Province harbours more endemic plant and animal taxa and more identifiable subspecies than any other area of comparable size in North America. We present evidence that physical historical processes have resulted in congruent patterns of genetic diversity over the past 2–10 million years. Using a molecular clock approach we show that diversification and establishment of spatial genetic structure across six taxonomic groups coincide with the putative age of Californias mountain ranges and aridification in the region. Our results demonstrate the importance of geographical barriers and climatological events to species diversification and the overall geographical structure of biodiversity. These results should facilitate conservation efforts in this biodiversity hotspot for taxa whose population genetic structure is still unknown and may suggest the potential utility of this approach in regional conservation planning efforts.

The quick and the dead: Correlational selection on morphology, performance, and habitat use in island lizards

Abstract Natural selection is an important driver of microevolution. Yet, despite significant theoretical debate, we still have a poor understanding of how selection operates on interacting traits (i.e., morphology, performance, habitat use). Locomotor performance is often assumed to impact survival because of its key role in foraging, predator escape, and social interactions, and shows strong links with morphology and habitat use within and among species. In particular, decades of study suggest, but have not yet demonstrated, that natural selection on locomotor performance has shaped the diversification of Anolis lizards in the Greater Antilles. Here, we estimate natural selection on sprinting speed and endurance in small replicate island populations of Anolis sagrei. Consistent with past correlational studies, long-limbed lizards ran faster on broad surfaces but also had increased sprint sensitivity on narrow surfaces. Moreover, performance differences were adaptive in the wild. Selection favored long-limbed lizards that were fast on broad surfaces, and preferred broad substrates in nature, and also short-limbed lizards that were less sprint sensitive on narrow surfaces, and preferred narrow perches in nature. This finding is unique in showing that selection does not act on performance alone, but rather on unique combinations of performance, morphology, and habitat use. Our results support the long-standing hypothesis that correlated selection on locomotor performance, morphology, and habitat use drives the evolution of ecomorphological correlations within Caribbean Anolis lizards, potentially providing a microevolutionary mechanism for their remarkable adaptive radiation.

Ocean currents mediate evolution in island lizards.

Islands are considered to be natural laboratories in which to examine evolution because of the implicit assumption that limited gene flow allows tests of evolutionary processes in isolated replicates. Here we show that this well-accepted idea requires re-examination. Island inundation during hurricanes can have devastating effects on lizard populations in the Bahamas. After severe storms, islands may be recolonized by over-water dispersal of lizards from neighbouring islands. High levels of gene flow may homogenize genes responsible for divergence, and are widely viewed as a constraining force on evolution. Ultimately, the magnitude of gene flow determines the extent to which populations diverge from one another, and whether or not they eventually form new species. We show that patterns of gene flow among island populations of Anolis lizards are best explained by prevailing ocean currents, and that over-water dispersal has evolutionary consequences. Across islands, divergence in fitness-related morphology decreases with increasing gene flow. Results suggest that over-water dispersal after hurricanes constrains adaptive diversification in Anolis lizards, and that it may have an important but previously undocumented role in this classical example of adaptive radiation.

Testing alternative mechanisms of evolutionary divergence in an African rain forest passerine bird.

Abstract Models of speciation in African rain forests have stressed either the role of isolation or ecological gradients. Here we contrast patterns of morphological and genetic divergence in parapatric and allopatric populations of the Little Greenbul, Andropadus virens, within different and similar habitats. We sampled 263 individuals from 18 sites and four different habitat types in Upper and Lower Guinea. We show that despite relatively high rates of gene flow among populations, A. virens has undergone significant morphological divergence across the savanna–forest ecotone and mountain–forest boundaries. These data support a central component of the divergence‐with‐gene‐flow model of speciation by suggesting that despite large amounts of gene flow, selection is sufficiently intense to cause morphological divergence. Despite evidence of isolation based on neutral genetic markers, we find little evidence of morphological divergence in fitness‐related traits between hypothesized refugial areas. Although genetic evidence suggests populations in Upper and Lower Guinea have been isolated for over 2 million years, morphological divergence appears to be driven more by habitat differences than geographic isolation and suggests that selection in parapatry may be more important than geographic isolation in causing adaptive divergence in morphology.

Experimentally assessing the relative importance of predation and competition as agents of selection

Field experiments that measure natural selection in response to manipulations of the selective regime are extremely rare, even in systems where the ecological basis of adaptation has been studied extensively. The adaptive radiation of Caribbean Anolis lizards has been studied for decades, leading to precise predictions about the influence of alternative agents of selection in the wild. Here we present experimental evidence for the relative importance of two putative agents of selection in shaping the adaptive landscape for a classic island radiation. We manipulated whole-island populations of the brown anole lizard, Anolis sagrei, to measure the relative importance of predation versus competition as agents of natural selection. We excluded or included bird and snake predators across six islands that ranged from low to high population densities of lizards, then measured subsequent differences in behaviour and natural selection in each population. Predators altered the lizards’ perching behaviour and increased mortality, but predation treatments did not alter selection on phenotypic traits. By contrast, experimentally increasing population density dramatically increased the strength of viability selection favouring large body size, long relative limb length and high running stamina. Our results from A. sagrei are consistent with the hypothesis that intraspecific competition is more important than predation in shaping the selective landscape for traits central to the adaptive radiation of Anolis ecomorphs.

Within-clutch variation in offspring sex determined by differences in sire body size: cryptic mate choice in the wild.

Sexual selection theory predicts that paternal quality should drive female investment in progeny. We tested whether polyandrous female side‐blotched lizards, Uta stansburiana, would adjust within‐clutch progeny investment according to sire phenotypes. In two different years, polyandrous females selectively used sperm from larger sires to produce sons and used sperm from smaller sires to produce daughters. This cryptic sperm choice had significant effects on progeny survival to maturity that were consistent with sexually antagonistic effects associated with sire body size. Large sires produced sons with high viability and small sires produced daughters with high viability. These results are consistent with our previous findings that alleles for male body size have different fitness effects in male and female progeny. Breeding experiments in the laboratory indicate that results from the wild are more likely due to female choice than biased sperm production by males. Our results demonstrate highly refined gender‐specific female choice for sperm and indicate that sire body size may signal the quality of sons or daughters that a sire will produce.

Genetic and maternal determinants of effective dispersal: the effect of sire genotype and size at birth in side-blotched lizards.

We assessed genetic factors on progeny dispersal due to sire color morph genotypes in a field pedigree and lab crosses, and we measured maternal effects by studying both natural and experimentally induced egg size variation. Progeny were released into nature upon hatching, but we recorded dispersal distance at maturity, which reflects effective dispersal after viability selection has run its course. Progeny dispersal was significantly affected by sire genotype. Progeny from orange sires dispersed the farthest. Progeny from blue sires dispersed intermediate distances. Progeny from yellow sires were the most philopatric. Sire genotype effects interacted with egg size. In particular, enlarged progeny from orange sires dispersed farther, while enlarged progeny from yellow sires were more philopatric. Progeny from blue sires were unaffected by egg size manipulations. Egg manipulations and natural variation generally had concordant effects indicative of causation. However, asymmetry of gigantization and miniaturization on progeny dispersal from some sire genotypes suggest the involvement of maternal factors besides egg size. Results of laboratory crosses with progeny released into nature confirmed key sire genotype effects and identified additional maternal effects that modulated dispersal as a function of progeny gender. We discuss the adaptive implications of progeny dispersal in the context of male (rock‐paper‐scissors) and female strategies (r‐ and K‐density cycle) that are associated with color morphs.

Uncoupling direct and indirect components of female choice in the wild

One of the most controversial debates in evolutionary biology concerns the fitness consequences of female choice in nature. Discriminating females may benefit from high-quality territories and/or sires with high-quality genes. Here we experimentally dissociate female preferences for high-quality territories and male body size in a wild population of side-blotched lizards, Uta stansburiana. Females preferred experimentally improved territories but still chose high-quality sires for their progeny. High-quality territories were associated with earlier egg-laying dates and larger eggs. These maternal effects, evidently stimulated by high-quality territories, have been shown to enhance competitive ability and therefore the likelihood that philopatric offspring will capitalize on the direct benefits of superior territories, previously shown to promote progeny growth rate and survival (most offspring do not disperse from their natal area). Paternity analysis within clutches co-sired by two males revealed that female preferences for large males were also adaptive in terms of indirect benefits. Females used sperm from large sires to produce sons and sperm from small sires to produce daughters. Differential allocation of resources and progeny sex was adaptive and demonstrates a high degree of female control in the mating system.

Testosterone, growth and the evolution of sexual size dimorphism

The integration of macroevolutionary pattern with developmental mechanism presents an outstanding challenge for studies of phenotypic evolution. Here, we use a combination of experimental and comparative data to test whether evolutionary shifts in the direction of sexual size dimorphism (SSD) correspond to underlying changes in the endocrine regulation of growth. First, we combine captive breeding studies with mark‐recapture data to show that male‐biased SSD develops in the brown anole lizard (Anolis sagrei) because males grow significantly faster than females as juveniles and adults. We then use castration surgeries and testosterone implants to show that castration inhibits, and testosterone stimulates, male growth. We conclude by reviewing published testosterone manipulations in other squamate reptiles in the context of evolutionary patterns in SSD. Collectively, these studies reveal that the evolution of SSD has been accompanied by underlying changes in the effect of testosterone on male growth, potentially facilitating the rapid evolution of SSD.