Jon Seger

Hedging one's evolutionary bets, revisited

Evolutionary bet-hedging involves a trade-off between the mean and variance of fitness, such that phenotypes with reduced mean fitness may be at a selective advantage under certain conditions. The theory of bet-hedging was first formulated in the 1970s, and recent empirical studies suggest that the process may operate in a wide range of plant and animal species.

Unifying genetic models for the evolution of female choice.

A best‐of‐N rule of female mating preferences can give rise to lines of unstable equilibria in a two‐locus haploid model of sexual selection. Under the best‐of‐N rule, which corresponds to choice at a lek, male fitnesses can exhibit a form of positive frequency‐dependence that is not seen under fixed‐relative‐preference rules (Kirkpatrick, 1982). This positive frequency‐dependence can be strongly destabilizing. Landes (1981) criterion for the stability of the equilibria in quantitative‐genetic models of sexual selection applies exactly and in general to the related family of simple population‐genetic models. This offers some insight into the workings of these models and greatly simplifies their analysis.

Kinship and covariance

Abstract Prices (1970) covariance theorem can be used to derive an expression for gene frequency change in kin selection models in which the fitness effect of an act is independent of the genotype of the recipient. This expression defines a coefficient of relatedness which subsumes r (Wright, 1922) , b (Hamilton, 1972) , ρ (Orlove & Wood, 1978) , and R (Michod & Hamilton, 1980) . The new coefficient extends the domain of Hamiltons rule to models in which the average gene frequency of actors differs from that of recipients.

Isotopic and genetic evidence for culturally inherited site fidelity to feeding grounds in southern right whales (Eubalaena australis)

Ocean warming will undoubtedly affect the migratory patterns of many marine species, but specific changes can be predicted only where behavioural mechanisms guiding migration are understood. Southern right whales show maternally inherited site fidelity to near‐shore winter nursery grounds, but exactly where they feed in summer (collectively and individually) remains mysterious. They consume huge quantities of copepods and krill, and their reproductive rates respond to fluctuations in krill abundance linked to El Niño Southern Oscillation (ENSO). Here we show that genetic and isotopic signatures, analysed together, indicate maternally directed site fidelity to diverse summer feeding grounds for female right whales calving at Península Valdés, Argentina. Isotopic values from 131 skin samples span a broad range (–23.1 to –17.2‰δ13C, 6.0 to 13.8‰δ15N) and are more similar than expected among individuals sharing the same mitochondrial haplotype. This pattern indicates that calves learn summer feeding locations from their mothers, and that the timescale of culturally inherited site fidelity to feeding grounds is at least several generations. Such conservatism would be expected to limit the exploration of new feeding opportunities, and may explain why this population shows increased rates of reproductive failure in years following elevated sea‐surface temperature anomalies off South Georgia, the richest known feeding ground for baleen whales in the South Atlantic.

Sex Ratios: Models of sex ratio evolution

Summary Our understanding of sex ratio evolution depends strongly on models that identify: (1) constraints on the production of male and female offspring, and (2) fitness consequences entailed by the production of different attainable brood sex ratios. Verbal and mathematical arguments by, among others, Darwin, Dusing, Fisher, and Shaw and Mohler established the fundamental principle that members of the minority sex tend to have higher fitness than members of the majority sex. They also outlined how various ecological, demographic and genetic variables might affect the details of sex-allocation strategies by modifying both the constraints and the fitness functions. Modern sex-allocation research is devoted largely to the exploration of such effects, which connect sex ratios to many other aspects of the biologies of many species. The models used in this work are of two general kinds: (1) expected-future-fitness or tracer-gene models that ask how a given sex allocation will affect the future frequencies of neutral genes carried by the allocating parent, and (2) explicit population-genetic models that consider the dynamics of alleles that determine alternative parental sex allocation phenotypes. Each kind of model has different strengths and weaknesses, and both are often essential to the full elucidation of a given problem. Introduction Males and females are produced in approximately equal numbers in most species with separate sexes, regardless of the mechanism of sex determination, and in most hermaphroditic species individuals expend approximately equal effort on male and female reproductive functions. Why should this be so?

Evolution of Sexual Systems and Sex Allocation in Plants when Growth and Reproduction Overlap

The common sexual systems in seed plants are hermaphroditism, dioecy, and gynodioecy. Here we attempt to explain this pattern by extending the ‘classical’ resource allocation model for the evolution of sexual systems. First we derive the equilibrium frequencies of all sex morphs and the sex allocations of hermaphrodites as functions of the male and female gain exponents, under the classical assumption that allocation takes place instantaneously from a fixed pool of resources. This analysis reveals two implications of the model that are not widely appreciated: (i) individuals of one sex (males or females) with a decelerating gain function may coexist with hermaphrodites when the gain function for the other sex is accelerating; and (ii) there are large regions of parameter space where the evolutionarily stable sexual system is subdioecy (a high frequency of one sex, with hermaphrodites whose allocation ratios are strongly biased toward the opposite sex function). Then we relax the unrealistic phenological assumption of the classical model and consider models where male allocation precedes female allocation, and where there are tradeoffs between growth and reproduction. When growth and reproduction overlap but there is no tradeoff between them, the predicted ESS sex allocations and sexual systems are identical to those of the classical model (for the same male and female gain exponents). But where there is a tradeoff, the ESS allocation ratios tend to be more female biased than in the classical model, and all three of the common sexual systems (but not androdioecy) can evolve where there is a saturating relation between investment in growth and realised growth.

Imprinting and paternal genome elimination in insects.

In many insects and other arthropods, males transmit only maternally inherited chromosomes (White 1973; Brown and Chandra 1977; Nur 1980, 1990a,b,c; Bell 1982; Bull 1983; Lyon and Rastan 1984; Lyon 1993; Wrensch and Ebbert 1993; Brun et al. 1995; Borsa and Kjellberg 1996). This remarkable genetic asymmetry can result from any of three principal systems of paternal genome exclusion, each of which has evolved several times. The most familiar and widespread exclusion system is arrhenotoky, in which fatherless males develop from unfertilized eggs and therefore lack paternal chromosomes at all stages of development. Most arrhenotokous systems are genetically haplodiploid, but a few are based on other modes of inheritance (see Nur 1980, 1990c; Bell 1982; Suomalainen et al. 1987). In the two other kinds of exclusion systems, a male’s paternally inherited chromosomes are actively eliminated: males begin life as seemingly conventional diploid zygotes but then either (1) lose their paternal chromosomes during embryonic development, becoming true maternal haploids (embryonic elimination), or (2) exhibit dramatically non-Mendelian patterns of meiosis and spermiogenesis, such that mature sperm carry only maternal chromosomes (germline elimination). To denote their formal (transmission-genetic) similarity to haplodiploid arrhenotoky, the embryonic and germline elimination systems are often characterized as parahaplodiploid or pseudoarrhenotokous.

Gene Genealogies Strongly Distorted by Weakly Interfering Mutations in Constant Environments

Neutral nucleotide diversity does not scale with population size as expected, and this “paradox of variation” is especially severe for animal mitochondria. Adaptive selective sweeps are often proposed as a major cause, but a plausible alternative is selection against large numbers of weakly deleterious mutations subject to Hill–Robertson interference. The mitochondrial genealogies of several species of whale lice (Amphipoda: Cyamus) are consistently too short relative to neutral-theory expectations, and they are also distorted in shape (branch-length proportions) and topology (relative sister-clade sizes). This pattern is not easily explained by adaptive sweeps or demographic history, but it can be reproduced in models of interference among forward and back mutations at large numbers of sites on a nonrecombining chromosome. A coalescent simulation algorithm was used to study this model over a wide range of parameter values. The genealogical distortions are all maximized when the selection coefficients are of critical intermediate sizes, such that Mullers ratchet begins to turn. In this regime, linked neutral nucleotide diversity becomes nearly insensitive to N. Mutations of this size dominate the dynamics even if there are also large numbers of more strongly and more weakly selected sites in the genome. A genealogical perspective on Hill–Robertson interference leads directly to a generalized background-selection model in which the effective population size is progressively reduced going back in time from the present.

Litter sex ratios in the golden hamster vary with time of mating and litter size and are not binomially distributed

SummaryPregnancy rates, litter sizes, and litter sex ratios vary strongly with the time in the estrous cycle at which female golden hamsters (Mesocricetus auratus) are mated. Early matings tend to produce relatively high pregnancy rates, large litters, and female-biased sex ratios, while late matings tend to produce low pregnancy rates, small litters, and male-biased sex ratios. Time of mating and litter size are therefore correlated, but each appears to have an independent effect on litter sex ratio: time of mating and sex ratio are positively correlated, holding litter size constant, while litter size and sex ratio are negatively correlated, holding time of mating constant. At each litter size greater than two, the variance of litter sex ratios is less than the binomial variance expected on the hypotheses of independent sampling with a constant probability of producing a male. The main features of the distribution of litter sex ratios can be generated from a causal model in which different probabilities of producing a male apply to “early” and “late” conceptions within each litter. The relationship between litter size and mean litter sex ratio is potentially consistent with several different models for the evolution of adaptive sex-ratio variation.

Partner choice and fidelity stabilize coevolution in a Cretaceous-age defensive symbiosis

Significance Symbiotic microbes are essential for the survival of many multicellular organisms, yet the factors promoting cooperative symbioses remain poorly understood. Three genera of solitary wasps cultivate antibiotic-producing Streptomyces bacteria for defense of their larvae against pathogens. Here we show that the wasp ancestor acquired the protective symbionts from the soil at least 68 million years ago. Although mother-to-offspring symbiont transmission dominates, exchange between unrelated individuals and uptake of opportunistic microorganisms from the environment occasionally occurs. However, experimental infections of female beewolves reveal that the wasps selectively block transmission of nonnative bacteria to their offspring. These findings suggest a previously unknown mechanism to maintain a specific symbiont over long evolutionary timescales and help to explain the persistence of bacterial mutualists in insects. Many insects rely on symbiotic microbes for survival, growth, or reproduction. Over evolutionary timescales, the association with intracellular symbionts is stabilized by partner fidelity through strictly vertical symbiont transmission, resulting in congruent host and symbiont phylogenies. However, little is known about how symbioses with extracellular symbionts, representing the majority of insect-associated microorganisms, evolve and remain stable despite opportunities for horizontal exchange and de novo acquisition of symbionts from the environment. Here we demonstrate that host control over symbiont transmission (partner choice) reinforces partner fidelity between solitary wasps and antibiotic-producing bacteria and thereby stabilizes this Cretaceous-age defensive mutualism. Phylogenetic analyses show that three genera of beewolf wasps (Philanthus, Trachypus, and Philanthinus) cultivate a distinct clade of Streptomyces bacteria for protection against pathogenic fungi. The symbionts were acquired from a soil-dwelling ancestor at least 68 million years ago, and vertical transmission via the brood cell and the cocoon surface resulted in host–symbiont codiversification. However, the external mode of transmission also provides opportunities for horizontal transfer, and beewolf species have indeed exchanged symbiont strains, possibly through predation or nest reuse. Experimental infection with nonnative bacteria reveals that—despite successful colonization of the antennal gland reservoirs—transmission to the cocoon is selectively blocked. Thus, partner choice can play an important role even in predominantly vertically transmitted symbioses by stabilizing the cooperative association over evolutionary timescales.