Modelling speciation: Problems and implications

Abstract

Darwin's and Wallace's 1859 explanation that novel speciation resulted from natural variants that had been subjected to selection was refined over the next 150 years as genetic inheritance and the importance of mutation-induced change were discovered, the quantitative theory of evolutionary population genetics was produced, the speed of genetic change in small populations became apparent and the ramifications of the DNA revolution became clear. This paper first discusses the modern view of speciation in its historical context. It then uses systems-biology approaches to consider the many complex processes that underpin the production of a new species; these extend in scale from genes to populations with the processes of variation, selection and speciation being affected by factors that range from mutation to climate change. Here, events at a particular scale level (e.g. protein network activity) are activated by the output of the level immediately below (i.e. gene expression) and generate a new output that activates the layer above (e.g. embryological development), with this change often being modulated by feedback from higher and lower levels. The analysis shows that activity at each level in the evolution of a new species is marked by stochastic activity, with mutation of course being the key step for variation. The paper examines events at each of these scale levels and particularly considers how the pathway by which mutation leads to phenotypic variants and the wide range of factors that drive selection can be investigated computationally. It concludes that, such is the complexity of speciation, most steps in the process are currently difficult to model and that predictions about future speciation will, apart from a few special cases, be hard to make. The corollary is that opportunities for novel variants to form are maximised.

Keywords: Evolution; selection; speciation; systems biology; variation (phenotypic).

Fig. 1

Ring species. The greenish warblers (Phylloscopus trochiloides) were originally present in the region south of the Himalayas. They slowly spread east and west forming a series of distinct species, eventually meeting up in Siberia to form a ring. All neighbouring species will interbreed except for those on either side of the meeting point. This seems to be because theirs songs are too different for the two species to recognise one another [6]. (Main image: Courtesy of G. Ambrus. Inserts: phylloscopus trochiloides: Courtesy of P. Jaganathan. P. t. plumbeitarsus: courtesy of Ayuwat Jearwattanakanok. P. t. viridanus: Courtesy of Dibenu Ash. (Other images published under a CC Attribution -Share Alike 3.0 unported License.)

Fig. 2

The process by which a new species eventually when a small founder population breaks away from a parent population (From [1], with permission).

Fig. 3

The scale hierarchy shows the key levels through which the effects of a mutation work their way up from the genome to the individual way. Note that there are feedback interactions, both up and down, between the levels. (From [1], with permission.)

Fig. 4

Protein networks that play important roles in animal development. a: The Epidermal growth factor (EGF) signalling pathway that often activates cell proliferation but has other roles. b: the Rho-GTPase network that directs morphogenesis through modulating cytoskeletal activity. The reasons why they should be so complicated are not known. (Courtesy of ProteinLounge, with permission).

Fig. 5

The effect of timing on the initiation of zebra striping patterns. 1: Three zebra species. a: Equus quagga burchelli has ∼26 stripes. b; E. zebra as ∼50 stripes. c: E. grevyi has ∼75 stripes. (a: Courtesy of Gusjr; published under a CC Attribution generic 2.0 license. b: Courtesy of Yathin S. Krishnappa; published under a CC Attribution share-alike 4.0 international license. c: Courtesy of Thivier; published under a CC Attribution share-alike 3.0 unported license.) 2a,b c: 3, 3.5 and 5 week horse embryos on which have been drawn stripes of 200um separation such as can be generated by reaction-diffusion kinetics. ai and aii: the effect of normal embryonic growth on stripes laid down at 3 weeks at 3,5 and 5 weeks. (From [51] with permission from John Wiley and sons).

Fig. 6

The effect of genetic drift in 12 large (N = 100) and 12 small (N = 10) populations that originally had equal numbers of red flour beetles (Trastaneum castaneum) with the dominant b⁺ allele and black flour beetles with the recessive genes (b^–/b^–). There was much more variation in the smaller populations and no obvious convergence to the extent that, in one of the small populations, the dominant gene was lost and the whole population ended up black. (From [55], with permission from the Society for the study of evolution (John Wiley Press) and thanks to John Herron for the redrawn and coloured image.)