Social status regulates growth rate: Consequences for life-history strategies

The life-history strategies of organisms are sculpted over evolutionary time by the relative prospects of present and future reproductive success. As a consequence, animals of many species show flexible behavioral responses to environmental and social change. Here we show that disruption of the habitat of a colony of African cichlid fish, Haplochromis burtoni (Günther) caused males to switch social status more frequently than animals kept in a stable environment. H. burtoni males can be either reproductively active, guarding a territory, or reproductively inactive (nonterritorial). Although on average 25–50% of the males are territorial in both the stable and unstable environments, during the 20-week study, nearly two-thirds of the animals became territorial for at least 1 week. Moreover, many fish changed social status several times. Surprisingly, the induced changes in social status caused changes in somatic growth. Nonterritorial males and animals ascending in social rank showed an increased growth rate whereas territorial males and animals descending in social rank slowed their growth rate or even shrank. Similar behavioral and physiological changes are caused by social change in animals kept in stable environmental conditions, although at a lower rate. This suggests that differential growth, in interaction with environmental conditions, is a central mechanism underlying the changes in social status. Such reversible phenotypic plasticity in a crucial life-history trait may have evolved to enable animals to shift resources from reproduction to growth or vice versa, depending on present and future reproductive prospects.

Spontaneous heterosis in larval life-history traits of hemiclonal frog hybrids

European water frog hybrids Rana esculenta (Rana ridibunda × Rana lessonae) reproduce hemiclonally, transmitting only their ridibunda genome to gametes. We compared fitness-related larval life-history traits of natural R. esculenta from Poland with those of the two sympatric parental species and of newly generated F1 hybrids. Compared with either parental species, F1 hybrid offspring had higher survival, higher early growth rates, a more advanced developmental stage by day 49, and earlier metamorphosis, but similar mass at metamorphosis. R. esculenta from natural lineages had trait values intermediate between those of F1 offspring and of the two parental species. The data support earlier observations on natural R. esculenta that had faster larval growth, earlier metamorphosis, and higher resistance to hypoxic conditions compared with either parental species. Observing larval heterosis in F1 hybrids in survival, growth rate, and time to metamorphosis, however, at an even higher degree than in hybrids from natural lineages, demonstrates that heterosis is spontaneous and results from hybridity per se rather than from subsequent interclonal selection; in natural lineages the effects of hybridity and of clonal history are confounded. This is compelling evidence for spontaneous heterosis in hybrid clonals. Results on hemiclonal fish hybrids (Poeciliopsis) showed no spontaneous heterosis; thus, our frog data are not applicable to all hybrid clonals. Our data do show, however, that heterosis is an important potential source for the extensively observed ecological success of hybrid clonals. We suggest that heterosis and interclonal selection together shape fitness of natural R. esculenta lineages.

Reproductive cooperation between queens and their mated workers: the complex life history of an ant with a valuable nest.

The life history of Harpegnathos saltator is exceptional among ants because both queens and workers reproduce sexually. Recently mated queens start new colonies alone, but later some of the offspring workers also become inseminated and take over the egg-laying role. This alternation seems associated with the existence of very complex underground nests, which are designed to survive floods. Longevity of ponerine queens is low (a consequence of limited caste dimorphism in this "primitive" subfamily), and upon the death of an H. saltator foundress, the nest represents a substantial investment. The queen's progeny should thus be strongly selected to retain the valuable nests. Unlike the flying queens, the workers copulate with males from their own colonies, and, thus, their offspring are expected to be highly related to the foundress. Colony fission appears not to occur because a daughter fragment would lack an adequate nest for protection. Thus, the annual production of queens in colonies with reproductive workers remains essential for the establishment of new colonies. This contrasts with various other ponerine species in which the queens no longer exist.

A modern human pattern of dental development in Lower Pleistocene hominids from Atapuerca-TD6 (Spain)

The study of life history evolution in hominids is crucial for the discernment of when and why humans have acquired our unique maturational pattern. Because the development of dentition is critically integrated into the life cycle in mammals, the determination of the time and pattern of dental development represents an appropriate method to infer changes in life history variables that occurred during hominid evolution. Here we present evidence derived from Lower Pleistocene human fossil remains recovered from the TD6 level (Aurora stratum) of the Gran Dolina site in the Sierra de Atapuerca, northern Spain. These hominids present a pattern of development similar to that of Homo sapiens, although some aspects (e.g., delayed M3 calcification) are not as derived as that of European populations and people of European origin. This evidence, taken together with the present knowledge of cranial capacity of these and other late Early Pleistocene hominids, supports the view that as early as 0.8 Ma at least one Homo species shared with modern humans a prolonged pattern of maturation.

Adaptive evolution of a candidate gene for aging in Drosophila

Examination of the phenotypic effects of specific mutations has been extensively used to identify candidate genes affecting traits of interest. However, such analyses do not reveal anything about the evolutionary forces acting at these loci, or whether standing allelic variation contributes to phenotypic variance in natural populations. The Drosophila gene methuselah (mth) has been proposed as having major effects on organismal stress response and longevity phenotype. Here, we examine patterns of polymorphism and divergence at mth in population level samples of Drosophila melanogaster, D. simulans, and D. yakuba. Mth has experienced an unusually high level of adaptive amino acid divergence concentrated in the intra- and extracellular loop domains of the receptor protein, suggesting the historical action of positive selection on those regions of the molecule that modulate signal transduction. Further analysis of single nucleotide polymorphisms (SNPs) in D. melanogaster provided evidence for contemporary and spatially variable selection at the mth locus. In ten surveyed populations, the most common mth haplotype exhibited a 40% cline in frequency that coincided with population level differences in multiple life-history traits including lifespan. This clinal pattern was not associated with any particular SNP in the coding region, indicating that selection is operating at a closely linked site that may be involved in gene expression. Together, these consistently nonneutral patterns of inter- and intraspecific variation suggest adaptive evolution of a signal transduction pathway that may modulate lifespan in nature.

Evolution of genome–phenome diversity under environmental stress

The genomic era revolutionized evolutionary biology. The enigma of genotypic-phenotypic diversity and biodiversity evolution of genes, genomes, phenomes, and biomes, reviewed here, was central in the research program of the Institute of Evolution, University of Haifa, since 1975. We explored the following questions. (i) How much of the genomic and phenomic diversity in nature is adaptive and processed by natural selection? (ii) What is the origin and evolution of adaptation and speciation processes under spatiotemporal variables and stressful macrogeographic and microgeographic environments? We advanced ecological genetics into ecological genomics and analyzed globally ecological, demographic, and life history variables in 1,200 diverse species across life, thousands of populations, and tens of thousands of individuals tested mostly for allozyme and partly for DNA diversity. Likewise, we tested thermal, chemical, climatic, and biotic stresses in several model organisms. Recently, we introduced genetic maps and quantitative trait loci to elucidate the genetic basis of adaptation and speciation. The genome–phenome holistic model was deciphered by the global regressive, progressive, and convergent evolution of subterranean mammals. Our results indicate abundant genotypic and phenotypic diversity in nature. The organization and evolution of molecular and organismal diversity in nature at global, regional, and local scales are nonrandom and structured; display regularities across life; and are positively correlated with, and partly predictable by, abiotic and biotic environmental heterogeneity and stress. Biodiversity evolution, even in small isolated populations, is primarily driven by natural selection, including diversifying, balancing, cyclical, and purifying selective regimes, interacting with, but ultimately overriding, the effects of mutation, migration, and stochasticity.

Age-specific inbreeding depression and components of genetic variance in relation to the evolution of senescence.

Two major theories of the evolution of senescence (mutation accumulation and antagonistic pleiotropy) make different predictions about the relationships between age, inbreeding effects, and the magnitude of genetic variance components of life-history components. We show that, under mutation accumulation, inbreeding decline and three major components of genetic variance are expected to increase with age in randomly mating populations. Under the simplest version of the antagonistic pleiotropy model, no changes in the severity of inbreeding decline, dominance variance, or the genetic variance of chromosomal homozygotes are expected, but additive genetic variance may increase with age. Age-specific survival rates and mating success were measured on virgin males, using lines extracted from a population of Drosophila melanogaster. For both traits, inbreeding decline and several components of genetic variance increase with age. The results are consistent with the mutation accumulation model, but can only be explained by antagonistic pleiotropy if there is a general tendency for an increase with age in the size of allelic effects on these life-history traits.

Does clutch size evolve in response to parasites and immunocompetence?

Parasites have been argued to influence clutch size evolution, but past work and theory has largely focused on within-species optimization solutions rather than clearly addressing among-species variation. The effects of parasites on clutch size variation among species can be complex, however, because different parasites can induce age-specific differences in mortality that can cause clutch size to evolve in different directions. We provide a conceptual argument that differences in immunocompetence among species should integrate differences in overall levels of parasite-induced mortality to which a species is exposed. We test this assumption and show that mortality caused by parasites is positively correlated with immunocompetence measured by cell-mediated measures. Under life history theory, clutch size should increase with increased adult mortality and decrease with increased juvenile mortality. Using immunocompetence as a general assay of parasite-induced mortality, we tested these predictions by using data for 25 species. We found that clutch size increased strongly with adult immunocompetence. In contrast, clutch size decreased weakly with increased juvenile immunocompetence. But, immunocompetence of juveniles may be constrained by selection on adults, and, when we controlled for adult immunocompetence, clutch size decreased with juvenile immunocompetence. Thus, immunocompetence seems to reflect evolutionary differences in parasite virulence experienced by species, and differences in age-specific parasite virulence appears to exert opposite selection on clutch size evolution.

Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life.

A symbiosis-based phylogeny leads to a consistent, useful classification system for all life. "Kingdoms" and "Domains" are replaced by biological names for the most inclusive taxa: Prokarya (bacteria) and Eukarya (symbiosis-derived nucleated organisms). The earliest Eukarya, anaerobic mastigotes, hypothetically originated from permanent whole-cell fusion between members of Archaea (e.g., Thermoplasma-like organisms) and of Eubacteria (e.g., Spirochaeta-like organisms). Molecular biology, life-history, and fossil record evidence support the reunification of bacteria as Prokarya while subdividing Eukarya into uniquely defined subtaxa: Protoctista, Animalia, Fungi, and Plantae.

Functional haplodiploidy: a mechanism for the spread of insecticide resistance in an important international insect pest.

The coffee berry borer, Hypothenemus hampei, is the most important insect pest of coffee worldwide and has an unusual life history that ensures a high degree of inbreeding. Individual females lay a predominantly female brood within individual coffee berries and because males are flightless there is almost entirely full sib mating. We investigated the genetics associated with this interesting life history after the important discovery of resistance to the cyclodiene type insecticide endosulfan. Both the inheritance of the resistance phenotype and the resistance-associated point mutation in the gamma-aminobutyric acid receptor gene Rdl were examined. Consistent with haplodiploidy, males failed to express and transmit paternally derived resistance alleles. Furthermore, while cytological examination revealed that males are diploid, one set of chromosomes was condensed, and probably nonfunctional, in the somatic cells of all males examined. Moreover, although two sets of chromosomes were present in primary spermatocytes, the chromosomes failed to pair before the single meiotic division, and only one set was packaged in sperm. Thus, the coffee berry borer is "functionally" haplodiploid. Its genetics and life history may therefore represent an interesting intermediate step in the evolution of true haplodiploidy. The influence of this breeding system on the spread of insecticide resistance is discussed.