What does it take to evolve behaviorally complex organisms?

What genotypic features explain the evolvability of organisms that have to accomplish many different tasks? The genotype of behaviorally complex organisms may be more likely to encode modular neural architectures because neural modules dedicated to distinct tasks avoid neural interference, i.e., the arrival of conflicting messages for changing the value of connection weights during learning. However, if the connection weights for the various modules are genetically inherited, this raises the problem of genetic linkage: favorable mutations may fall on one portion of the genotype encoding one neural module and unfavorable mutations on another portion encoding another module. We show that this can prevent the genotype from reaching an adaptive optimum. This effect is different from other linkage effects described in the literature and we argue that it represents a new class of genetic constraints. Using simulations we show that sexual reproduction can alleviate the problem of genetic linkage by recombining separate modules all of which incorporate either favorable or unfavorable mutations. We speculate that this effect may contribute to the taxonomic prevalence of sexual reproduction among higher organisms. In addition to sexual recombination, the problem of genetic linkage for behaviorally complex organisms may be mitigated by entrusting evolution with the task of finding appropriate modular architectures and learning with the task of finding the appropriate connection weights for these architectures

On the nature of thumbs

Differential Hox gene expression make the thumb specia

Quasi-Independence, Homology and the Unity of Type: A Topological Theory of Characters

In this paper Lewontin’s notion of “quasi-independence” of characters is formalized as the assumption that a region of the phenotype space can be represented by a product space of orthogonal factors. In this picture each character corresponds to a factor of a region of the phenotype space. We consider any region of the phenotype space that has a given factorization as a “type”, i.e. as a set of phenotypes that share the same set of phenotypic characters. Using the notion of local factorizations we develop a theory of character identity based on the continuation of common factors among different regions of the phenotype space. We also consider the topological constraints on evolutionary transitions among regions with different regional factorizations, i.e. for the evolution of new types or body plans. It is shown that direct transition between different “types” is only possible if the transitional forms have all the characters that the ancestral and the derived types have and are thus compatible with the factorization of both types. Transitional forms thus have to go over a “complexity hump” where they have more quasi-independent characters than either the ancestral as well as the derived type. The only logical, but biologically unlikely, alternative is a “hopeful monster” that transforms in a single step from the ancestral type to the derived type. Topological considerations also suggest a new factor that may contribute to the evolutionary stability of “types”. It is shown that if the type is decomposable into factors which are vertex irregular (i.e. have states that are more or less preferred in a random walk), the region of phenotypes representing the type contains islands of strongly preferred states. In other words types have a statistical tendency of retaining evolutionary trajectories within their interior and thus add to the evolutionary persistence of types

Cell-type phylogenetics and the origin of endometrial stromal cells

SummaryA challenge of genome annotation is the identification of genes performing specific biological functions. Here, we propose a phylogenetic approach that utilizes RNA-seq data to infer the historical relationships among cell types and to trace the pattern of gene-expression changes on the tree. The hypothesis is that gene-expression changes coincidental with the origin of a cell type will be important for the function of the derived cell type. We apply this approach to the endometrial stromal cells (ESCs), which are critical for the initiation and maintenance of pregnancy. Our approach identified well-known regulators of ESCs, PGR and FOXO1, as well as genes not yet implicated in female fertility, including GATA2 and TFAP2C. Knockdown analysis confirmed that they are essential for ESC differentiation. We conclude that phylogenetic analysis of cell transcriptomes is a powerful tool for discovery of genes performing cell-type-specific functions

Adaptive evolution of Hox-gene homeodomains after cluster duplications

BACKGROUND: Hox genes code for homeodomain-containing transcription factors that function in cell fate determination and embryonic development. Hox genes are arranged in clusters with up to 14 genes. This archetypical chordate cluster has duplicated several times in vertebrates, once at the origin of vertebrates and once at the origin of gnathostoms, an additional duplication event is associated with the origin of teleosts and the agnanths, suggesting that duplicated Hox cluster genes are involved in the genetic mechanisms behind the diversification of vertebrate body plans, and the origin of morphological novelties. Preservation of duplicate genes is promoted by functional divergence of paralogs, either by subfunction partitioning among paralogs or the acquisition of a novel function by one paralog. But for Hox genes the mechanisms of paralog divergence is unknown, leaving open the role of Hox gene duplication in morphological evolution. RESULTS: Here, we use several complementary methods, including branch-specific d(N)/d(S )ratio tests, branch-site d(N)/d(S )ratio tests, clade level amino acid conservation/variation patterns, and relative rate ratio tests, to show that the homeodomain of Hox genes was under positive Darwinian selection after cluster duplications. CONCLUSION: Our results suggest that positive selection acted on the homeodomain immediately after Hox clusters duplications. The location of sites under positive selection in the homeodomain suggests that they are involved in protein-protein interactions. These results further suggest that adaptive evolution actively contributed to Hox-gene homeodomain functions

Divergence of Conserved Non-Coding Sequences: Rate Estimate and Relative Rate Tests

In many eukaryotic genomes only a small fraction of the DNA codes for proteins, but the non-protein coding DNA harbors important genetic elements directing the development and the physiology of the organisms, like promoters, enhancers, insulators, and micro-RNA genes. The molecular evolution of these genetic elements is difficult to study because their functional significance is hard to deduce from sequence information alone. Here we propose an approach to the study of the rate of evolution of functional non-coding sequences at a macro-evolutionary scale. We identify functionally important non-coding sequences as Conserved Non-Coding Nucleotide (CNCN) sequences from the comparison of two outgroup species. The CNCN sequences so identified are then compared to their homologous sequences in a pair of ingroup species, and we monitor the degree of modification these sequences suffered in the two ingroup lineages. We propose a method to test for rate differences in the modification of CNCN sequences among the two ingroup lineages, as well as a method to estimate their rate of modification. We apply this method to the full sequences of the HoxA clusters from six gnathostome species: a shark, Heterodontus francisci; a basal ray finned fish, Polypterus senegalus; the amphibian, Xenopus tropicalis; as well as three mammalian species, human, rat and mouse. The results show that the evolutionary rate of CNCN sequences is not distinguishable among the three mammalian lineages, while the Xenopus lineage has a significantly increased rate of evolution. Furthermore the estimates of the rate parameters suggest that in the stem lineage of mammals the rate of CNCN sequence evolution was more than twice the rate observed within the placental amniotes clade, suggesting a high rate of evolution of cis-regulatory elements during the origin of amniotes and mammals. We conclude that the proposed methods can be used for testing hypotheses about the rate and pattern of evolution of putative cis-regulatory elements

Gene phylogenies and protein–protein interactions: possible artifacts resulting from shared protein interaction partners

The study of gene families critically depends on the correct reconstruction of gene genealogies, as for instance in the case of transcription factor genes like Hox genes and Dlx gene families. Proteins belonging to the same family are likely to share some of the same protein interaction partners and may thus face a similar selective environment. This common selective environment can induce co-evolutionary pressures and thus can give rise to correlated rates and patterns of evolution among members of a gene family. In this study, we simulate the evolution of a family of sequences which share a set of interaction partners. Depending on the amount of sequence dedicated to protein–protein interaction and the relative rate parameters of sequence evolution three outcomes are possible: if the fraction of the sequence dedicated to interaction with common co-factors is low and the time since divergence is small, the trees based on sequence information tend to be correct. If the time since gene duplication is long two possible outcomes are observed in our simulations. If the rate of evolution of the interaction partner is small compared to the rate of evolution of the focal protein family, the reconstructed trees tend towards star phylogenies. As the rate of evolution of the interaction partner approaches that of the focal protein family the reconstructed phylogenies tend to be incorrectly resolved. We conclude that the genealogies of gene families can be hard to estimate, in particular if the proteins interact with a conserved set of binding partners, as is likely the case for transcription factors

The Evolution of HoxD-11 Expression in the Bird Wing: Insights from Alligator mississippiensis

BACKGROUND:Comparative morphology identifies the digits of the wing of birds as 1,2 and 3, but they develop at embryological positions that become digits 2, 3 and 4 in other amniotes. A hypothesis to explain this is that a homeotic frame shift of digital identity occurred in the evolution of the bird wing, such that digits 1,2 and 3 are developing from embryological positions 2, 3 and 4. Digit 1 of the mouse is the only digit that shows no late expression of HoxD-11. This is also true for the anterior digit of the bird wing, suggesting this digit is actually a digit 1. If this is the case, we can expect closer relatives of birds to show no HoxD-11 expression only in digit 1. To test this prediction we investigate HoxD-11 expression in crocodilians, the closest living relatives of birds. METHODOLOGY/PRINCIPAL FINDINGS:Using degenerate primers we cloned a 606 nucleotide fragment of exon 1 of the alligator HoxD-11 gene and used it for whole-mount in-situ detection in alligator embryos. We found that in the pentadactyl forelimbs of alligator, as in the mouse, late expression of HoxD-11 is absent only in digit 1. CONCLUSIONS/SIGNIFICANCE:The ancestral condition for amniotes is that late-phase HoxD-11 expression is absent only in digit 1. The biphalangeal morphology and lack of HoxD-11 expression of the anterior digit of the wing is like digit 1 of alligator and mouse, but its embryological position as digit 2 is derived. HoxD-11 expression in alligator is consistent with the hypothesis that both digit morphology as well as HoxD-11 expression are shifted towards posterior in the bird wing