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  Multicellular development is thought to have arisen independently multiple of times in the eukaryotic tree of life. In amoebozoa, a striking example is found in cellular slime mold Dictyostelium discoideum where an aggregate of cells form a fruitingbody by directed cell migration and positional rearrangements. While the initial aggregative stage is dictated by GPCR-mediated chemotaxis to extracellular cAMP, what follows next remains a mystery. Differentiating prespore and prestalk cells appear at random positions then sort out to form the ‘tip’- the critical organizing center of this organism. Here by using microfluidics gradient chambers and microspheres coated with Ig-domain containing membrane protein TgrC1, we show that directed migration is mediated by constitutive membrane localization of the Scar/WAVE complex at the cell-cell contact sites. Surprisingly, the mechanism is an inversion of the so-called contact inhibition of locomotion – a canonical scheme of cell guidance that underlie collective cell migration in metazoans. Furthermore, we demonstrate that both prestalk and prespore cells can protrude towards the contact signal as well as to chemotax towards cAMP, however when given both signals, prestalk cells orient towards the chemoattractant whereas prespore cells choose the contact signal. These data suggest a new model of cell sorting by two competing cues and modes of collective cell migration. The present findings cast light on the remarkable parallels in collective cell migration that evolved independently in metazoa and amoebozoa.