Journal of Evolutionary Biology最新文献

Darwin argued that natural selection leads organisms to appear as if they are striving to maximise their fitness. This idea is readily recognised at the individual cell or body level, but such adaptive design may also manifest at some higher levels of biological organisation. Previous work has formalised the idea that social groups can be viewed as adaptive individuals in their own right-i.e., 'superorganisms'-under the assumptions that within-group selection is absent and that there is no class structure. However, the original and most common biological use of the term 'superorganism' is in reference to insect colonies in which members exhibit striking class structure in the form of reproductive division of labour. Accordingly, although obligately eusocial colonies are regularly conceptualised as having the capacity for colony-level adaptation, current formalisms are unable to support this idea. Here, we develop a formal theory of group-level adaptation for obligately eusocial colonies by establishing mathematical correspondences that connect the dynamics of natural selection-as described by Price's equation-to the mathematics of optimisation-wherein the colony is considered a fitness-maximising agent-under a range of assumptions as to which members of the colony control its phenotype and the degree to which they are genetically related.

Characterizing morphological variation along the vertebral column of mammals is commonly investigated at a broad phylogenetic scale, leaving within-species variation understudied due to the requirement of larger sample sizes. This leads to a knowledge gap of how variation within species relates to morphological diversity among species. Here, we overcome these limitations and examine the morphological variation at the within-species level in the vertebral column of 4 species-equivalent groups of rabbits and hares. We then expanded to the among-species levels of the family Leporidae, the order Lagomorpha, and broadly among terrestrial placentals. We sampled 9 vertebrae along the vertebral column of each specimen. Using a geometric morphometric approach, we calculated the Procrustes variance of vertebrae shapes and used this as an index for the extent of morphological variation of each vertebra along the vertebral column, which we call the profile. We find that the profile of morphological variation along the column differs among species and between phylogenetic levels; among-species variation is not simply a scaled-up profile of the within-species level. We highlight that by adopting the multi-level analysis, we can better understand how the mammalian vertebral column can evolve.

Batesian mimicry has been regarded as classic evidence of adaptation by natural selection, in which a palatable species avoids predation by resembling unpalatable species. In some butterfly species, Batesian mimicry is female-limited and mimetic females coexist with male-like (nonmimetic) females. Why do nonmimetic females continue to exist despite the possible differential predation pressure? One possible hypothesis is a trade-off between the anti-predatory defence and mating success. Specifically, mimetic females may be less attractive to conspecific males as they look like heterospecific butterflies. However, empirical studies based on behavioural data have shown mixed results. Here, we directly investigated female mating frequency by counting spermatophores and compared it between mimetic and nonmimetic females in a Batesian mimetic butterfly, Papilio polytes. The mating frequencies of the two types of females were almost identical in all four studied populations. More than 99% of females copulated at least once regardless of morph. In addition, the spermatophore counts increased with age and did not differ between morphs. Our results strongly suggest that the anti-predatory traits are unlikely to be costly to the reproductive success of mimetic P. polytes females, providing no support for the sexual selection hypothesis regarding maintenance of mimetic polymorphism.

Inbreeding plays a strong role in shaping life-history traits and behaviours. Supporting evidence for this role often comes from observational studies. Experiments that establish causality and formally test how environmental factors moderate any effects of inbreeding remain underutilized. We ran an experiment to test how developmental temperature and inbreeding influence key life-history traits (growth rate, size and age at maturity, survival, and sex ratio) and locomotor behaviours (boldness and habituation) in juvenile guppies (Poecilia reticulata). We used a controlled breeding design to generate inbred and outbred individuals that were then reared under a control (26 °C) or an elevated temperature (30 °C) until maturity. Developmental temperature strongly affected life-history traits; both sexes matured earlier at 30 °C, but only males exhibited slower early growth and reduced size at maturity. Female growth and size at maturity were unaffected. The higher developmental temperature reduced boldness in both sexes; however, only females at 26 °C habituated to the novel test environment. In contrast, inbreeding had no significant effects on any of the measured traits, nor did it significantly interact with temperature. In sum, under our experimental conditions, developmental temperature is the primary driver of phenotypic plasticity in guppies, generating sex-specific responses in both life-history traits and behaviour, while inbreeding between siblings had no detectable effects on any of the measured traits. Our findings highlight the key role of temperature in shaping developmental and behavioural trajectories, and reveal that a single generation of inbreeding may not always affect life-history traits, even under environmental stress.

The major histocompatibility complex (MHC) is a gene cluster essential for pathogen recognition in jawed vertebrates. It encompasses the MHC class I genes which primarily recognize intracellular parasites, and the MHC class II genes which primarily recognize extracellular parasites. In wild birds, most studies investigating associations between MHC variants and parasites have been carried out in passerines, and have repeatedly shown that specific MHC class I variants provide resistance to intracellular haemosporidian parasites. In contrast, research on the associations between MHC variants and parasites in non-passerine birds remains limited. In this study, we examined the association between MHC-IIB supertypes and the bacterial load of a sexually transmitted bacterium (named C34) in the black-legged kittiwake (Rissa tridactyla), a genetically monogamous seabird. We focused on MHC class II genes because extracellular parasites are particularly prevalent in non-passerines and may therefore exert strong selection on the studied host. We found that females with lower C34 load had better reproductive performance, and higher probability to carry the MHC-IIB supertype SUP6. In contrast, in males, we observed a positive association between C34 load and reproductive performance, but no association between C34 load and MHC-IIB supertypes. While sexually transmitted diseases are not expected to be a strong selective force in genetically monogamous species, our study suggests that C34 might exert a selective pressure on the evolution of the MHC-IIB. Therefore, further research should explore the influence of sexually transmitted diseases on the reproductive biology of genetically monogamous species.

Organisms often face a fundamental trade-off between growth and predator avoidance, where traits that enhance growth-such as higher activity rates-also increase predation risk. While many species reduce activity in response to predators, potentially constraining growth, this trade-off can be mitigated if alternative traits, such as resource digestive efficiency, compensate for reduced activity. Such trait compensation could enable organisms to minimize growth costs while evading predators. To test this idea, we combined a mesocosm experiment with lab-based digestive physiological assays to examine survival selection and plasticity in damselfly larvae exposed to fish predators. We found that selection favoured less active individuals, yet this reduction in activity did not suppress growth. Instead, plastic increases in consumption rate, selection for greater assimilation efficiency, and weaker digestive stress responses allowed individuals to maintain growth despite reduced activity and elevated metabolic rates. Our results reveal that selection on digestive physiology can buffer organisms against the putative costs of predator avoidance, demonstrating how trait networks can decouple growth from predation risk in complex ecological systems.

Male fertility in plants is often controlled by the interaction between mitochondrial and nuclear genes. Some mitotypes confer cytoplasmic male sterility (CMS), making the individual male-sterile, unless the nuclear background contains alleles called restorers, which suppress the effects of CMS and restore the hermaphroditic phenotype. Restorers in cultivated crops are often alleles with strong and dominant effect, but in wild plants, data often suggest more complex systems. Here, we characterized the inheritance and specificity of restoration in a new CMS model, the freshwater snail Physa acuta. We explored two different populations: (i) a naive population, i.e., without contact with CMS in the past 80 generations, and (ii) a non-naive population, where CMS is present and largely restored. Although we found male fertility of individuals with CMS mitogenomes to be heritable in both contexts, this genetic determinism was of a different nature depending on population history. In naive populations not coevolved with CMS, the background variation may include alleles that happen to act as weak quantitative modifiers of the penetrance of CMS, while in populations coevolved with CMS, selection may have favoured, when such variants were available, the emergence of strong alleles with a dominant effect.

Maternal effects (the consistent effect of a mother on her offspring) can inflate estimates of additive genetic variation ($V_{A}$) if not properly accounted for. As they are typically assumed to cause similarities only among maternal siblings, they are often accounted for by modelling maternal identity effects. However, if maternal effects have a genetic basis, they create additional similarities among relatives with related mothers that are not captured by maternal identity effects. Unmodelled maternal genetic variance ($V_{Mg}$) may therefore still inflate $V_{A}$ estimates in common quantitative genetic models, which is underappreciated in the literature. Using published data and simulations, we explore the extent of this problem. Published estimates from 8 species suggest that a large proportion of total maternal variation ($V_{M}$) is genetic ($sim$65%). Both these data and simulations confirmed that unmodelled $V_{Mg}$ can cause overestimation of $V_{A}$ and underestimation of $V_{M}$, the bias increasing with the proportion of non-sibling maternal relatives in a pedigree. Simulations show these biases are further influenced by the size and direction of any direct-maternal genetic covariance. The estimation of total additive genetic variation ($V_{A_t}$; the weighted sum of $V_{A}$ and $V_{Mg}$) is additionally affected, limiting inferences about evolutionary potential from simple maternal effects models. Unbiased estimates require modelling $V_{Mg}$ explicitly, but these models are often avoided due to perceived data limitations. We demonstrate that estimating $V_{Mg}$ is possible even with small pedigrees, reducing bias in $V_{A}$ estimates, and maintaining accuracy in estimates of $V_{A}$, $V_{M}$, and $V_{A_t}$. We therefore advocate for the broader use of these models.

The universality of the trade-off between fecundity and longevity in life-history theory is sometimes contested. Social insects present the arguably strongest challenge, as (i) queens not only monopolize reproduction, but also live much longer than workers, and (ii) within a caste, those individuals that lay more eggs are also observed to live longer. Positive fecundity-longevity relationships can appear in observational data even though an underlying trade-off exists, as individual variation in resource acquisition (e.g., variation in habitat quality) can mask the trade-off. Here, we demonstrate theoretically that the fecundity-longevity trade-off in social insects can be easily masked even without differences in individual quality. Demographic stochasticity, caused by variable worker lifespans, leads to self-reinforcing dynamics (equivalent to the well-known Matthew effect), where "lucky" colonies exhibit healthy growth and long-lived, productive queens, while "unlucky" colonies show the opposite combination of traits. Allocation variation between individual queens, if present, can unmask the trade-off in principle, but the trade-off remains commonly concealed not only when measuring fecundity as a cumulative total (a strongly confounded measure as longer-lived queens have more time to produce eggs), but also when measuring fecundity as a rate. Our results help align superorganismal fitness components with general life-history principles, and highlight the necessity of experimental manipulations when making statements regarding trade-offs or the lack thereof.

Genomic differentiation usually accompanies speciation, but that differentiation is often highly heterogeneous across the genome. Understanding what parts of the genome are more prone to differentiation can inform us about genomic regions and evolutionary processes that may be central to the speciation process. Here, we study genomic variation among 3 hybridizing species of North American woodpecker: red-breasted, red-naped, and yellow-bellied sapsuckers (Sphyrapicus ruber, S. nuchalis, and S. varius). We use whole genome resequencing to measure genetic variation among these species and to quantify how the level of differentiation varies across the genome. We find that regions of high relative differentiation between species (FST) tend to have low absolute nucleotide distance between species (πB), indicating that regions of high relative differentiation often have more recent between-population coalescence times than regions of low relative differentiation do. Most of the high-FST genomic windows are found on the Z chromosome, pointing to this sex chromosome as being particularly important in sapsucker differentiation and potentially speciation. These results are consistent with a model of speciation in which selective sweeps of globally advantageous variants spread among partly differentiated populations, followed by differential local adaptation of those same genomic regions. We propose that sapsucker speciation may have occurred primarily via this process occurring on the Z chromosomes, resulting in genetic incompatibilities involving divergent Z chromosomes.